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CONTRIBUTIONS 


TO   THE 


STUDY  OF  THE  BEHAVIOR 
OF  LOWER  ORGANISMS 


BY 


HERBERT  S.  JENNINGS 

Assistant  Professor  of  Zoology,  University  of  Pennsylvania 
Research  Assistant,  Carnegie  Institution  of  [Vashington 


Published  by  the  Carnegie  Institution 

OF  Washington 

1904 


CONTRIBUTIONS 

TO  THE 

STUDY  OF  THE  BEHAVIOR 
OF  LOWER  ORGANISMS 


BY 


HERBERT  S,  JENNINGS 

Assistant  Professor  of  Zoology,  University  of  Pennsylvania 
Research  Assistant,  Carnegie  Institution  of  Washington 


Published  by  the  Carnegie  Institution 

OF  Washington 

1904 


Carnegie  Institution  of  Washington^ 
Publication  No.  i6. 


Press  of  Gibson  Bros., 
Washington,  D.  C. 


> 


v 


zrs 


PREFATORY  NOTE. 


The  investigations  the  results  of  which  are  herein  set  forth  were 
carried  out  by  the  aid  of  certain  grants  from  the  Carnegie  Institution 
of  Washington.  The  author  desires  to  express  his  deep  sense  of  obli- 
gation for  the  aid  thus  rendered.  The  first  five  papers  were  prepared 
at  the  Zoological  Laboratory  of  the  University  of  Michigan,  and  were 
submitted  to  the  Carnegie  Institution  for  publication  August  i,  1903. 
To  the  third  paper  some  additions  were  made  in  February,  1904. 
The  sixth  and  seventh  papers  were  prepared  at  the  Naples  Zoological 
Station,  while  the  writer  was  acting  as  Research  Assistant  of  the 
Carnegie  Institution,  and  were  transmitted  for  publication  in  January 
and  March,  respectively,  1904. 


LIST  OF  PAPERS. 

1.  Reactions  to  Heat  and  Cold  in  the  Ciliate  Infusoria. 

2.  Reactions  to  Light  in  Ciliates  and  Flagellates. 

3.  Reactions  to  Stimuli  in  Certain  Rotifera. 

4.  The  Theory  of  Tropisms. 

5.  Physiological    States   as    Determining   Factors    in    the  Behavior  of   Lower 

Organisms. 

6.  The  Movements  and  Reactions  of  Amoeba. 

7.  The  Method  of  Trial  and  Error  in  the  Behavior  of  Lower  Organisms. 


FIRST    PAPER 


REACTIONS  TO  HEAT  AND  GOLD 
IN  THE  CILIATE  INFUSORIA. 


5  '' 


REACTIONS  TO  HEAT  AND  COLD  IN  THE 
CILIATE   INFUSORIA. 


To  explain  the  movements  of  organisms  toward  or  from  a  source  of 
stimulus,  we  find  given  almost  universally  in  one  shape  or  another  a 
certain  general  formula.  This  is  the  schema  set  forth,  with  unessen- 
tial variations,  by  Verworn  (1899,  pp.  500-502)  for  the  orientation  of 
a  ciliate  or  flagellate  infusorian  to  a  one-sided  stimulus,  and  by  Loeb 
(1897,  pp.  439-442)  for  the  tropisms  of  organisms  in  general.  Essen- 
tially, the  schema  is  as  follows :  An  agent  acting  upon  the  organism 
from  one  side  causes  the  locomotor  organs  of  that  side  to  contract 
either  more  strongly  or  less  strongly  than  those  of  the  opposite  side. 


Fig.  I.* 

In  the  former  case  (Fig.  i)  the  animal  is  turned  away  from  the  source 
of  stimulus,  till  it  comes  into  a  position  in  which  the  motor  organs  of 
the  two  sides  are  similarly  affected.  Then  progressing  straight  for- 
ward, it  of  course  moves  away  from  the  source  of  stimulus  (negative 
taxis  or  tropism) .  If  the  motor  organs  on  the  side  most  affected  are 
caused  to  contract  less  strongly  than  those  on  the  opposite  side  (Fig.  2) 


♦Fig.  I. — Diagram  of  a  negative  reaction  of  an  organism,  according  lo  the 
tropism  schema.  The  motor  organs  which  act  more  eflfectively  are  shown  more 
heavily  drawn.  The  more  pointed  end  is  the  anterior.  A  stimulus  is  supposed 
to  impinge  upon  the  organism  a  from  the  direction  indicated  by  arrows;  this 
causes  the  motor  organs  directly  affected  by  the  stimulus  to  beat  more  strongly, 
as  indicated  by  the  darker  shade.  The  result  is  to  turn  the  anterior  end  in  the 
direction  indicated  by  curved  arrows.  The  organism  thus  occupies  successively 
the  positions  «,  b,  c,  finally  coming  into  the  position  d.  Here  the  motor  organs 
of  the  two  sides  are  equally  affected  by  the  stimulus,  hence  there  is  no  further 
cause  for  a  change  of  position.  The  usual  forward  motion  of  the  organism  now 
takes  it  away  from  the  source  of  stimulus,  as  indicated  by  the  straight  arrow  at  d. 

7 


O  THE  BEHAVIOR  OF  LOWER  OKGAN'ISMS. 

the  organism  is  necessarily  turned  with  anterior  end  toward  the  source 
of  stimulus ;  then  its  usual  forward  movements  take  it  toward  the 
source  of  stimulus  (positive  taxis  or  tropism).  Loeb  lays  especial 
stress  on  the  direction  from  which  the  stimulus  comes,  as  it  is  this 
that  determines  which  side  shall  be  most  strongly  affected  by  the 
stimulus  ;  otherwise  the  theory  as  he  sets  it  forth  is  essentially  like  that 
held  by  Verworn.  Both  these  authors  apply  this  schema  to  the  move- 
ments of  organisms  to  and  from  many  sorts  of  stimuli,  making  it  a 
general  formula  for  taxis  or  tropisms.     Verworn  says  (1899,  p.  503): 

Thus  the  phenomena  of  positive  and  negative  chemotaxis,  thermotaxis,  photo- 
taxis  and  galvanotaxis,  which  are  so  highly  interesting  and  important  in  all  or- 
ganic life,  follow  with  mechanical  necessity  as  the  simple  results  of  differences 
in  biotonus,  which  are  produced  by  the  action  of  stimuli  at  two  different  poles  of 
the  free  living  cell. 

In  the  present  series  of  papers  the  writer  proposes  to  examine  the 
behavior  of  a  number  of  lower   organisms,   in   order   to   determine 


O: 


Fig.  2.* 

whether  the  reactions  to  the  usual  stimuli  take  place  in  accordance 
with  this  tropism  schema  or  not,  and  if  not,  to  determine  the  real 
nature  of  the  reaction  method.  In  this  first  paper  we  shall  deal  with 
reactions  to  heat  and  cold. 

In  his  recent  series  of  papers  on  the  reactions  of  infusoria  to  heat  and 
cold,  Mendelssohn  (1902,  «,  <5,  c)  develops  a  theory  of  thermotaxis  in 
accordance  with  the  general  theory  of  tropisms,  above  set  forth.  In  an 
earlier  paper  (Jennings,  1899)  *^^  present  author,  on  the  other  hand, 


♦Fig.  2. — Diagram  of  a  positive  reaction,  according  to  the  tropism  schema. 
A  stimulus  coming  from  the  direction  indicated  by  the  arrows  to  the  right  acts 
upon  the  organism  a.  The  effect  of  the  stimulus  is  to  cause  the  motor  organs 
directly  affected  by  it  to  contract  less  strongly,  as  indicated  by  the  lighter  shade 
on  the  right  side  of  a.  As  a  result  the  animal  is  turned  as  shown  by  the  curved 
arrows,  occupying  successively  the  positions  a,  b,  c,  d.  At  d  the  stimulus 
affects  the  two  sides  alike,  hence  there  is  no  cause  for  further  turning,  and  the 
usual  forward  movement  of  the  organism  takes  it  toward  the  source  of  stimulus. 


REACTIONS  TO  HEAT  AND  COLD. 


gave  a  brief  account  of  the  reactions  of  Paramecium  to  heat  and  cold, 
according  to  which  these  reactions  are  quite  inconsistent  with  the 
tropism  schema.  As  the  matter  is  one  of  considerable  interest,  and  the 
conclusions  reached  by  Mendelssohn  and  myself  seem  quite  irrecon- 
cilable, I  have  examined  anew  the  phenomena  in  a  considerable  number 
of  infusoria,  including  Paramecium. 

The  general  phenomena  to  be  explained  are  well  seen  in  the  follow- 
ing experiment,  taken  from  Mendelssohn  (Fig.  3).  An  ebonite  trough 
10  cm.  in  length  and  2  cm.  wide  is  filled  with  water  containing  Para- 
mecia  (a).  Now,  by  proper  methods,  one  end  of  the  trough  is  slowly 
heated  to  38°,  while  the  other  is  kept  at  the  temperature  26°.     The 


JO'  — -  i>5-° 

Fig.  3.* 

Paramecia  soon  leave  the  heated  region,  traveling  away  from  it  in  a 
rather  compact  mass,  and  in  5  to  15  minutes  they  have  reached  the  op- 
posite end  (6) .  If  now  the  temperature  at  the  two  ends  is  reversed, 
the  Paramecia  travel  back  to  the  end  from  which  they  came.  If  the 
temperature  is  lowered  to  10°  at  one  end,  instead  of  raised,  similar  re- 
sults are  obtained ;  the  Paramecia  leave  the  cold  region,  as  before  they 

*  Fig.  3.— General  phenomena  of  thermotaxis  in  Paramecium,  after  Men- 
delssohn (1902,  a).  At  a  the  Paramecia  are  placed  in  an  ebonite  trough,  both 
ends  of  which  have  a  temperature  of  19°.  The  Paramecia  are  equally  scattered. 
At  d,  the  temperature  of  one  end  is  raised  to  38"^,  while  at  the  other  it  is  only  26°. 
The  Paramecia  collect  at  the  end  having  the  lower  temperature  ("  negative 
thermotaxis").  At  c,  one  end  has  a  temperature  of  25°,  while  the  other  is 
lowered  to  10°.  The  Paramecia  now  gather  at  the  end  having  the  higher  tem- 
perature ("positive  thermotaxis"). 


lO  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

left  the  heated  region  (c).  If  one  end  is  heated,  while  the  other  is 
cooled,  the  Paramecia  gather  in  the  intermediate  region. 

How  are  these  movements  to  be  explained  ?  Mendelssohn  applies 
to  the  phenomena  Verworn's  schema  for  the  orientation  of  a  ciliate 
organism  to  a  one-sided  stimulus  (see  Figs,  i  and  2).  As  we  wish  to 
deal  thoroughly  with  this  schema,  it  will  be  well  to  set  it  forth  here,  as 
applied  by  Mendelssohn  to  heat  and  cold,  with  some  fullness. 

The  temperature  being  higher  at  one  end  of  the  trough  than  at  the 
other,  that  side  or  end  of  the  animal  directed  to  the  heated  end  of  the 
trough  has  a  higher  temperature  than  has  the  opposite  side  or  end 
(see  Fig.  4).  This  difference  in  temperature  causes  a  difference  in  the 
beat  of  the  cilia.  In  negative  thermotaxis  the  higher  temperature 
causes  the  cilia  to  contract  more  strongly,  as  indicated  by  the  heavier 
shade  (on  the  left  side)  in  the  figure ;  hence  the  animal  is  turned 
toward  the  opposite  side,  or  away  from  the  source  of  heat,  until  it 
comes  into  a  position  where  the  heat  acts  equally  on  the  two  sides. 
The  Paramecium  then  of  course  has  its  anterior  end  directed  from  the 

heated  region,  and  its  ordinary 


swimming  carries  it  away.  In 
positive  thermotaxis,  on  the 
other  hand,  the  lower  tempera- 
ture causes  stronger  contrac- 
YiG.  4*  tions ;  hence  the  cilia  on  the 

side  next  the  cold  region  con- 
tract more  strongly,  turning  the  anterior  end  in  the  opposite  direction. 
The  Paramecium  then  swims  away,  as  a  result  of  its  normal  forward 
movement. 

Mendelssohn  studied  the  subject  primarily  from  a  quantitative  stand- 
point, determining  the  optimum  temperature,  the  rate  of  reaction,  the 
effects  of  different  temperatures,  etc.  For  this  purpose  he  constructed 
a  very  ingenious  and  delicate  apparatus,  which  permitted  accurate 
quantitative  results.  Relying  then  upon  his  valuable  papers  for  these 
matters,  I  have  devoted  myself  entirely  to  a  study  of  the  mechanism  of 
the  reactions.     For  this  purpose  an  apparatus  was  used  that  is  similar 


*  Fig.  4. — Diagram  of  the  thermotactic  reaction  of  Paramecium  as  conceived 
by  Mendelssohn,  after  Mendelssohn  (1902,  b).  The  heavier  cilia  on  the  left  side 
show  those  contracting  most  strongly  and  hence  those  most  effective  in  turning 
the  organism  or  driving  it  forward.  In  negative  thermotaxis  the  left  end  would 
have  the  higher  temperature,  causing  the  cilia  of  the  left  side  of  the  organism 
a  to  beat  more  strongly.  As  a  result,  the  organism  turns,  occupying  suc- 
cessively the  positions  a,  b,  c,  d.  In  the  latter  position  there  is  no  further 
cause  for  turning,  and  the  animal  swims  directly  away  from  the  heated  end. 
The  same  diagram  illustrates  also  positive  thermotaxis,  if  the  left  end  is  sup- 
posed to  be  cooled  below  the  optimum. 


REACTIONS    TO    HEAT    AND    COLD. 


IC 


in  principle  to  that  of  Mendelssohn,  but  more  easily  constructed  and 
permitting  exact  observation  of  the  organisms  with  the  microscope, 
though  otherwise  much  less  elegant  than  Mendelssohn's.  This  ap- 
paratus is  shown  in  Fig.  5.  It  consists  essentially  of  three  glass  tubes, 
of  8  millimeters  bore,  which  are  supported  in  a  horizontal  position, 
side  by  side,  by  passing  them  through  auger  holes  in  a  block  of 
wood.  The  tubes  are  one  inch  apart  and  are  placed  exactly  at 
the  same  level,  so  that  a  glass  slide  rests  equally  on  all  three.  To 
the  two  ends  of  each  of  these  rubber  tubes  are  attached.  The  rubber 
tubes  from  one  end  pass  upward  into  vessels  of  water  raised  on  a  shelf 
above  the  level  of  the  apparatus.     From  the  other  end  the  rubber  tubes 


Fig.  5.* 

pass  downward  into  a  waste  pail,  thus  acting  as  overflow  tubes.  A 
trough,  or  slide  (5),  containing  infusoria,  is  placed  on  the  three  glass 
tubes ;  the  water  in  the  vessels  on  the  shelf  is  heated  or  cooled  to  any 
desired  temperature,  and  is  then  siphoned  off  and  allowed  to  flow 
downward  through  the  glass  tubes.  The  rate  of  flow  is  controlled  by 
pinchcocks.  In  this  manner  heated  water  can  be  caused  to  flow 
beneath  one  end  of  the  slide,  cold  water  beneath  the  other.  The  slide 
being  thus  unequally  warmed,  the  reactions  of  the  organisms  can  be 
observed.  The  rubber  tubes  leading  from  the  hot  and  cold  vessels  can 
be  interchanged,  so  that  the  temperature  at  either  end  or  the  middle  of 
the  slide  can  be  at  once  changed  and  made  high  or  low,  without  the 


*  Fig.  5. — Apparatus   used   for   testing   reaction  to  heat  and  cold, 
scription,  see  text. 


For  de- 


12  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

slightest  disturbance  to  the  slide  or  trough  containing  the  organisms. 
The  plan  of  this  apparatus  is  taken  from  that  of  Mendelssohn.  It  can 
be  readily  constructed  in  an  hour  or  less,  and  gives  essentially  the  same 
results  as  Mendelssohn's  more  elaborate  arrangement.  With  the  use 
of  specially  constructed  thermometers,  such  as  were  employed  by 
Mendelssohn,  exactly  the  same  quantitative  work  could  be  done.  The 
present  apparatus  has  the  advantage  that  it  is  possible  to  place  a 
mirror  beneath  the  glass  slide  or  trough  bearing  the  organisms,  and 
thus  to  observe  the  movements  of  the  latter  with  the  microscope  by  the 
aid  of  reflected  light.  With  the  long-armed  Braus-Driiner  stand  the 
whole  extent  of  the  trough  can  be  examined  at  ease,  and  the  movements 
of  the  organisms  accurately  observed  with  the  stereoscopic  binocular. 

As  a  trough  I  usually  employed  a  glass  slide,  to  which  strips  of  glass 
2  mm.  in  diameter  had  been  cemented,  making  a  trough  3  inches  long, 
about  two-thirds  of  an  inch  wide,  and  2  mm.  deep.  In  some  of  the 
experiments  the  trough  was  covered  with  a  glass  plate ;  in  others  it 
was  left  open.     Both  methods  have  their  advantages  and  disadvantages. 

To  realize  the  exact  conditions  under  which  the  organisms  are  act- 
ing it  is  necessary  to  consider  a  further  question  :  What  is  the  precise 
nature  of  the  stimulating  agent  in  these  experiments.?  Are  we  dealing 
with  radiant  heat  or  with  conducted  heat.?  If  we  are  dealing 
primarily  with  radiant  heat,  of  course  currents  in  the  water  have 
no  effect  on  the  distribution  of  the  stimulating  agent.  If,  on  the  other 
hand,  we  are  dealing  with  conducted  heat,  if  the  stimulating  agent  is 
the  heated  or  cooled  water,  then  the  conditions  are  different.  Local 
currents  will  cause  local  variations  in  the  distribution  of  the  heated 
water.  It  is  evident,  I  think,  that  the  second  alternative  is  in  all 
probability  the  correct  one.  Certainly  in  a  bath-tub  or  in  a  long 
vessel  of  any  sort  in  which  the  water  is  heated  at  one  end  and  not  at 
the  other,  it  is  possible  by  producing  currents  to  vary  the  distribution 
of  the  heated  water  and  to  perceive  with  the  hand  that  it  is  this  heated 
water  which  acts  as  the  stimulus. 

The  importance  of  these  considerations  is  evident  when  we  take  into 
account  the  fact  that  the  ciliate  infusoria  are  always  accompanied  by 
currents  of  typical  character,  having  a  definite  relation  to  the  form  and 
orientation  of  the  animal's  body.  As  a  result  of  these  currents,  the  in- 
fusorian  becomes  not  a  mere  passive  recipient  of  stimulations,  but  an 
active  agent,  determining  by  its  activity  how  and  in  what  part  of  the 
body  it  shall  be  affected  by  stimuli.  This  may  be  illustrated  by  a 
diagram  (Fig.  6)  showing  the  typical  currents  produced  by  the  cilia 
of  Paramecium  and  the  effect  produced  by  these  currents  upon  the 
distribution  of  the  heated  (or  cooled)  water.     The  temperature  is  con- 


REACTIONS    TO    HEAT    AND    COLD. 


13 


ceived  to  be  greatest  to  the  right  of  the  figure  and  to  fall  off  regu- 
larly toward  the  left,  the  lines  indicating  regions  of  equal  temperature. 
The  last  line  to  the  left  is  marked  28°,  this  being  about  the  threshold 
temperature  for  the  negative  reaction  of  Paramecium,  according  to 
Mendelssohn.  The  space  about  the  Paramecium  (without  lines)  is  at 
a  temperature  below  28° — say  at  the  room  temperature — so  that  it 
does  not  act  as  a  stimulus  to  cause  movement.      Now,  as  the  diagram 


Fig.  6.* 

shows,  a  cone  of  water  is  drawn  toward  the  anterior  end  of  Para- 
mecium, from  a  considerable  distance  away,  necessarily  therefore 
including  water  above  the  threshold  temperature  of  28°.    This  cone  or 


*FiG.  6. — Diagram  of  currents  produced  bv  the  cilia  in  Paramecium  when 
the  animal  is  nearly  or  quite  at  rest.  At  right  of  the  line  marked  28°  the  tem- 
perature is  above  the  optimum  (above  28°)  while  at  the  left  of  this  line  it  is  at 
the  normal  or  optimum  temperature.  The  heated  water  first  reaches  the  Para- 
mecium at  the  anterior  end  on  the  oral  side,  passing  down  the  oral  groove  to 
the  mouth. 


14  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

vortex  of  water  passes  as  a  slender  stream  along  the  oral  groove  of 
Paramecium  to  the  mouth.  Consequently,  water  heated  above  the 
threshold  temperature  reaches  the  Paramecium  in  this  region  before  it 
touches  the  body  elsewhere.  The  result  is  thus  a  stimulation  on  the 
oral  side  of  the  body,  not  elsewhere. 

Thus  the  way  in  which  the  organism  is  stimulated  depends  not  ex- 
clusively on  the  physical  laws  of  the  distribution  of  heat,  but  upon  the 
activity  of  the  organism  ;  and  the  method  of  reaction,  as  we  shall  see, 
is  of  a  corresponding  character. 

It  is  not  difficult  to  observe  the  distribution  of  the  currents  above 
described  if  one  adds  to  the  water  on  one  side  of  the  nearly  or  quite 
quiet  infusorian  a  cloud  of  very  finely  ground  India  ink.  The  same 
results  are  obtained  with  other  infusoria ;  in  Stentor,  in  Bursaria,  and 
in  some  of  the  larger  Hypotricha  the  results  are  particularly  striking. 
Of  course  if  the  India  ink,  or  the  surface  of  threshold  temperature,  is 
advancing  obliquely  to  the  axis  of  the  infusoria,  the  results  are  more 
complicated,  and  a  diagram  such  as  we  have  in  Fig.  6  is  not  easy  to 
construct.  But  the  result  is  uniformly  to  bring  the  stimulating  agent 
to  the  peristome  before  it  reaches  any  other  part  of  the  body.  It  is  not 
possible  to  observe  directly  the  distribution  of  water  of  different  tem- 
peratures, but  under  the  influence  of  currents  this  of  course  follows, 
essentially,  the  same  laws  as  do  fine  particles  suspended  in  the  water. 

Another  factor  which  it  is  important  to  take  into  consideration  in 
studying  the  effects  of  heat  or  other  agents  on  the  infusoria  is  the 
greater  sensitiveness  of  the  anterior  end  and  oral  surface  (or  peristome) 
as  compared  with  the  remainder  of  the  body.  This  the  present  writer 
has  demonstrated  for  the  anterior  end  by  direct  mechanical  stimulation 
in  a  considerable  number  of  infusoria  (Jennings,  1900),  while  Roesle 
(1902)  has  shown  a  similar  high  comparative  sensitivity  for  the  peri- 
stome region.  The  difference  is  such  that  in  many  cases  where  the 
animal  is  completely  enveloped  by  a  stimulating  agent  (as  by  a  chemi- 
cal, or  by  warm  or  cold  water)  there  is  reason  to  think  that  the 
reaction  given  is  due  to  the  stimulation  at  these  regions  alone.  In 
other  words,  the  stimulus  reaches  its  threshold  value  for  the  anterior 
end  and  the  region  about  the  mouth  much  before  it  reaches  this  value 
for  the  rest  of  the  body.  This  consideration  has  an  important  bearing 
on  the  theory  which  is  frequently  maintained,  that  the  directive  action 
of  a  stimulus  is  due  to  the  difference  in  its  intensity  on  the  two  ends  or 
sides  of  the  organism.  Even  if  a  stimulating  agent  acts,  fer  se^ 
slightly  more  strongly  on  the  posterior  end  than  on  the  anterior  end 
of  an  infusorian,  there  is  reason  to  think  that  the  reaction  would  be 
conditioned  entirely  by  the  stimulus  at  the  anterior  end,  this  reaching 


REACTIONS    TO    HEAT    AND    COLD.  1 5 

its  threshold  value  before  the  stimulus  elsewhere  produces  any  effect. 
Corresponding  statements  could  be  made  with  relation  to  the  oral  and 
aboral  sides.  Of  course,  owing  to  the  course  of  the  currents  above 
described,  any  stimulating  agent  whose  distribution  is  affected  by  cur- 
rents in  the  water  will  usually  reach  the  anterior  end  and  oral  side 
first  in  any  case. 

Summing  up,  we  find  (i)  that  the  threshold  intensity  of  a  stimulating 
agent  whose  distribution  is  affected  by  currents  in  the  water  will  reach 
the  anterior  end  and  oral  side  of  the  organism  before  it  reaches  other 
parts  of  the  body ;  (2)  that  the  anterior  end  and  oral  surface  are  more 
sensitive  than  the  rest  of  the  body,  so  that  the  threshold  value  for^ 
stimuli  is  less  here  than  elsewhere. 

We  may  now  proceed  to  an  account  of  the  observed  method  by 
which  some  of  the  organisms  react  to  heat  and  cold. 

Oxytricha  fallax :  This  is  one  of  the  most  favorable  of  the  Ciliata 
for  determining  the  method  of  reactions  to  stimuli,  for  two  reasons, 
(i)  It  is  easily  procurable  in  large  numbers,  occurring  in  cultures  of 
the  same  sort  that  produce  Paramecium,  and  in  equal  abundance. 
(2)  It  does  not,  as  a  rule,  revolve  rapidly  on  its  long  axis,  as  Para- 
mecium does,  but  usually  creeps  with  its  oral  or  ventral  side  against  a 
surface,  so  that  it  is  not  difficult  to  observe  the  relation  of  the  reaction 
movements  to  the  differences  in  the  sides  of  the  body. 

When  water  containing  a  large  number  of  Oxytrichas  is  placed  in 
the  trough  and  one  end  of  the  trough  is  heated  by  passing  warm  water 
through  the  tube  which  underlies  it,  the  Oxytrichas  gradually  pass 
toward  the  opposite  end  of  the  trough,  forming  a  dense  assemblage 
with  a  rather  sharply  defined  edge  toward  the  heated  side.  If  the  end 
at  first  heated  is  now  cooled  and  the  opposite  end  heated,  the  organisms 
pass  back  to  the  end  from  which  they  first  came.  Similar  results  are 
obtained  by  making  one  end  very  cold ;  the  animals  gather  in  an 
optimum  region,  avoiding  both  too  great  heat  and  too  great  cold.* 
The  phenomena  are  identical  with  what  is  to  be  observed  in  the  case 
of  Paramecium,  save  that  it  requires  somewhat  longer  for  the  Oxytrichas 
to  move  from  one  end  of  the  trough  to  the  other,  and  the  progress  in  a 
definite  direction  is  not  so  steady  as  we  find  it  in  Paramecium. 

If  the  movements  of  the  individuals  are  observed  we  find  them  to  be 
as  follows :    Near  that   end  of  the  trough  where  the  temperature  is 


*  Many  quantitative  data  for  various  infusoria  are  given  in  the  valuable  papers 
of  Mendelssohn.  As  the  object  of  the  present  paper  was  not  to  obtain  quantita- 
tive data,  but  to  determine  just  how  the  animals  acted,  absolute  temperatures 
are  not  recorded.  In  every  case  the  experiments  were  so  varied  as  to  use  at 
times  temperatures  to  which  a  reaction  was  hardly  noticeable;  at  other  times 
more  extreme  temperatures,  up  to  those  which  were  destructive. 


/ 


i6 


THE    BEHAVIOR   OF    LOWER    ORGANISMS. 


raised  above  the  threshold  vahie  the  animals  begin  to  move  about 
rapidly.  At  first  view  this  movement  seems  to  be  quite  irregular,  as 
Mendelssohn  describes  it  in  Paramecium.     But  exact  observation  of 


Fig.  7.* 

the  individuals  taken  separately  shows  that  this  movement  is  not  so 
entirely  irregular  as  it  at  first  appears.     Most  of  the  animals  swim 

•Fig.  7.— Method  by  which  Oxytricha  fallax  reacts  to  heat  or  cold.  The  fig- 
ure represents  one  end  of  a  trough  or  slide,  which  is  heated  from  the  end  x.  An 
Oxytricha  in  the  position  i  is  reached  by  the  heat  coming  from  the  end  *.     The 


REACTIONS   TO    HEAT   AND   COLD.  1 7 

backward,  circling  at  the  same  time  toward  the  right  or  aboral  side,  as 
shown  in  Fig.  7.  This  lasts  but  a  moment ;  then  the  animal  swims 
forward,  at  the  same  time  turning  to  the  right  or  aboral  side.  That  is, 
the  individuals  give  the  typical  motor  reaction,  as  described  in  the  fifth 
of  my  studies  (Jennings,  1900).  This  reaction  is  repeated  many 
times,  as  long  indeed  as  the  animal  remains  in  the  heated  region.  But 
of  course  this  movement  scatters  the  animals  rapidly.  Those  that 
strike  against  the  end  or  sides  of  the  trough  repeat  the  reaction  above 
described,  backing,  turning  to  the  right,  then  going  forward  (Fig.  7  at 
8,  9,  10,  II).  They  thus  become  directed  in  some  other  way.  Those 
that  are  directed  away  from  the  heated  region  pass  into  cooler  water 
and  hence  no  longer  give  the  reaction,  but  continue  their  course  (Fig. 
7  at  13,  14).  The  result  is  that  the  individuals  which  swim  away  from 
the  heated  end  continue  their  course,  while  those  starting  in  any  other 
direction  are  stopped  and  turned  (through  the  motor  reaction),  until 
they  too  get  started  away  from  the  heated  region.  Thus  after  a  time 
there  is  a  steady  stream  of  organisms  swimming  or  creeping  away  from 
the  heated  end,  while  there  is  no  regular  movement  in  any  other 
direction.  In  this  manner  arises  the  orientation  of  the  animals,  with 
anterior  ends  directed  away  from  the  heated  region. 

The  movements  of  the  individuals  are  exactly  as  above  described 
even  when  the  heat  is  applied  some  distance  from  the  region  where 
the  animal  is  found  and  gradually  approaches  it  from  one  side.  The 
animal  by  no  means  turns  directly  away  from  the  heated  region,  but 
repeatedly  gives  the  backing  and  turning  reaction  till  it  is  finally  mov- 
ing in  a  direction  which  takes  it  out  of  the  heated  region. 

How  is  this  continued  backing  and  turning  to  be  accounted  for  on 
the  theory  of  direct  action  on  the  locomotor  organs  of  the  two  sides  as 
maintained  by  Mendelssohn.?  This  author  speaks  in  the  case  of  Para- 
mecium merely  of  "disordered"  movements  when  the  reaction  first 


animal  reacts  by  turning  to  the  right  and  backing  (i,  2,  3),  turning  again  (3-4), 
swimming  forward  (4-5),  backing  (5-6),  turning  again  to  the  right  C6-7),  etc., 
till  it  comes  against  the  wall  of  the  trough  (8).  It  then  reacts  as  before,  by 
backing  (8-9),  turning  to  the  right  (9-10).  This  type  of  reaction  continues  as 
long  as  the  Oxytricha  is  in  the  heated  region,  or  as  long  as  its  movements  carry 
it  either  against  the  wall  or  into  the  heated  region.  When  it  finally  becomes 
directed  away  from  the  heated  region  (13),  as  it  must  in  time  if  it  continues  its 
reactions,  it  swims  forward,  and  since  it  is  no  longer  stimulated,  it  no  longer 
reacts.  When  large  numbers  of  animals  react  in  this  way,  in  the  course  of 
time  nearly  all  become  pointed  in  the  same  direction,  as  at  13  or  14,  so  that  a 
marked  "orientation"  is  produced.  Thus  orientation  is  produced  by  ''ex- 
clusion," due  to  the  fact  that  the  organism  is  prevented,  either  by  the  heat  or 
the  walls  of  the  trough,  from  swimming  in  any  other  direction. 


l8  THE    BRHAVIOR    OF    LOWER    ORGANISMS. 

begins,  and  thinks  this  is  due  to  "  individual  differences,  or  to  ill- 
defined  internal  causes,  or  perhaps  rather  to  the  heterogeneity  of  the 
medium  in  which  they  find  themselves"  (Mendelssohn,  1902,  c,  p. 
492),  and  that  it  has  nothing  to  do  with  thermotaxis  proper.  This  is 
typical  of  many  of  the  statements  made  concerning  the  behavior  of  the 
lower  organisms ;  the  movements,  so  long  as  they  do  not  agree  with 
the  preconceived  schema,  are  cast  aside  as  disordered,  and  attention  is 
called  only  to  the  movements  that  do  not  conflict  with  the  theory. 
Thus  Mendelssohn  says  that  this  disordered  movement  ''  ceases  im- 
mediately as  soon  as  the  thermotactic  action  manifests  itself"  (/.  c,  p. 
492).  This  is  true  merely  because  the  thermotactic  action  is  conceived 
to  begin  only  after  the  organism  has,  through  the  movements  above 
described,  gotten  itself  into  such  a  position  that  it  moves  away  from 
the  heated  region.  Of  course  if  all  movements  except  those  after 
orientation  has  occurred  are  thrown  out  of  consideration,  the  orientation 
can  be  accounted  for  in  any  way  desired. 

In  Paramecium,  for  which  alone  Mendelssohn  attempts  to  give  an 
account,  based  on  observation,  of  the  mechanism  of  the  thermotactic 
response,  the  exact  character  of  the  movements  is  undoubtedly  diflicult 
to  observe.  This  animal  is  nearly  cylindrical  in  section  ;  the  oral  side 
is  very  slightly  marked,  the  movements  are  rapid,  and  the  animal  con- 
tinually revolves  rapidly  on  its  long  axis,  so  that  observation  of  the 
relation  of  the  direction  of  turning  to  the  differentiations  of  the  body  is 
very  difficult.  In  Oxytricha  and  other  Hypotricha  these  difficulties 
are  almost  absent ;  the  body  is  markedly  differentiated  ;  the  movements 
are  less  rapid,  and,  most  important  of  all,  there  is  usually  no  revolu- 
tion on  the  long  axis.  It  is  unfortunate  therefore  that  Mendelssohn 
included  none  of  the  Hypotricha  among  the  organisms  which  he 
studied.  With  careful  observation  of  the  movements  of  individuals 
the  mechanism  of  the  reactions  is  in  these  animals  absolutely  clear. 

A  crucial  test  of  the  theory  of  direct  orientation  as  maintained  by 
Mendelssohn  is  given  by  observation  of  the  direction  in  which  the 
animals  turn  in  becoming  oriented.  Mendelssohn  (1902,  c,  p.  492) 
says  that  after  the  disordered  movements  *'  the  movements  executed  to 
place  the  body  in  orientation  are  rather  movements  of  rotation."  This 
could  hardly  be  otherwise,  but  the  important  question  for  deciding  as 
to  the  nature  of  the  reaction  is.  How  does  the  rotation  take  place?  Is 
it  determined  by  the  direction  from  which  the  heat  comes,  as  required 
by  Mendelssohn's  theory,  or  is  it  determined  by  the  differentiations  of 
the  animal's  body  ?  This  point  is  a  decisive  one  for  interpreting  the 
nature  of  the  reaction.  Suppose  we  have  an  Oxytricha  in  the  position 
a-a,  Fig.  8,  and  heat  is  applied  in  such  a  way  as  to  reach  the  organism 


REACTIONS    TO    HEAT    AND    COLD. 


19 


from  the  direction  indicated  by  the  straight  arrows.  The  heat  is  supra- 
optimal,  so  that  the  organism  moves  away  from  it.  In  what  direction 
will  the  organism  turn  in  order  to  reach  the  position  of  orientation 
h'b}  According  to  the  theory  of  Mendelssohn,  that  the  orientation 
is  due  to  an  increase  of  the  effective  beat  of  the  cilia  on  the  side  from 
which  the  heat  comes,  the  animal  must  turn  in  the  direction  indicated 
by  the  arrow  x^  and  this  is  of  course  what  one  would  naturally 
expect,  since  this  is  the  most  direct  method  of  becoming  oriented. 
But  as  a  matter  of  fact  the  organism  turns  in  the  opposite  direction,  as 
indicated  by  the  arrow  jk,  thus  demonstrating  the  incorrectness  of  the 
theory  that  orientation  is  due  to  increase  of  the  effective  beat  of  the 
cilia  on  the  side  from  which  the  heat  comes.  I  have  made  this  obser- 
vation hundreds  of  times,  not  only  upon  Oxytricha,  but  on  other 
Hypotricha  and  on  infu- 
soria belonging  to  other 
groups  (see  below).  The 
direction  of  turning  is  de- 
termined, under  the  heat 
stimulus,  by  the  differen- 
tiation of  the  animal's 
body.  Oxytricha  turns  to 
the  right,  without  regard 
to  the  direction  from  which 
the  heat  comes.  This  is 
very  striking  when  the 
trough  is  covered  and  part 
of  the  animals  are  creep- 
ing on  the  cover-glass  with 
ventral  side  up,  while  the  remainder  are  creeping  on  the  bottom  of  the 
trough  with  ventral  side  down.  When  stimulated  by  heat  approaching 
from  one  side,  all  the  members  of  the  first  group  will  be  observed  to 
turn  counter  clock-wise,  while  those  of  the  second  group  turn  in  the 
same  direction  as  the  clock  hands  ;  that  is,  each  specimen  turns  toward 
its  right  side. 

For  becoming  completely  oriented  an  animal  in  the  position  a-a  in 
Fig.  8  usually  requires  a  number  of  reactions,  as  indicated  in  Fig.  7, 
but  the  turning  in  every  case  is  as  indicated  by  the  arrowy  (Fig.  8). 

After  it  has  become  oriented  with  the  anterior  end  away  from  the 
source  of  heat,  Oxytricha  by  no  means  maintains  this  position  with 
rigidity  ;  on  the  contrary  the  individuals  shoot  back  and  forth,  in  a  way 
that  might  be  anticipated  from  the  method  in  which  the  reaction 
occurs.     They  thus  form  groups  here  and  there,  which  gradually  move 


Fig.  8.— Method  of  orientation  in  Oxytricha. 

For  details,  see  text. 


20  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

away  from  the  heat,  much  as  is  described  by  Mendelssohn  for  Para- 
tnccium  bursaria.  With  a  large  number  of  individuals  a  general 
orientation  is  evident,  however,  after  the  experiment  has  been  some 
time  in  progress. 

If  ice  water  is  used  as  the  stimulating  agent  in  place  of  heated  water, 
the  phenomena  to  be  observed  are  practically  identical  with  those 
above  described.  The  organisms  leave  the  colder  region,  giving  the 
same  reaction  as  with  heated  water.  As  the  cold  has  the  additional 
effect  of  decreasing  the  movements,  many  individuals  are  immobilized 
by  a  very  low  temperature  before  they  have  succeeded  in  escaping 
from  it,  so  that  they  remain  in  the  cold  region.  The  reaction  is  thus 
less  clearly  defined  than  that  to  heat. 

Oxytricka  ceruginosa :  This  organism,  though  smaller,  is  in  some 
respects  more  favorable  than  O.  fallax  for  observing  the  method  of 
reaction.  This  is  because  the  individuals  are  more  inclined  to  swim 
freely  through  the  water,  so  that  their  progress  away  from  or  toward 
the  heated  region  is  more  rapid  than  in  O.  fallax.  O.  ceruginosa^ 
further,  even  when  moving  freely  through  the  water,  either  does  not 
revolve  on  the  long  axis  at  all  or  revolves  only  very  slowly.  In  con- 
sequence of  this  it  is  easy  to  determine  the  relation  of  the  direction  of 
turning  to  the  differentiations  of  the  body. 

The  reaction  to  heat  and  cold  is  in  essentials  identical  with  that  of 
O.  fallax^  and  this  reaction  is  repeated  till  the  animals  are  carried  into 
a  region  where  the  temperature  is  not  such  as  to  cause  the  reaction. 
Those  that  are  carried  into  such  a  region  will  of  course  be  swimming 
away  from  the  stimulating  region  ;  hence,  in  a  large  number  of  individ- 
uals there  is  an  evident  orientation,  with  anterior  end  directed  away 
from  the  source  of  heat  or  cold.  All  the  conditions  and  details  as  to 
the  production  of  this  orientation  are  as  set  forth  above  for  O.  fallax. 

Stylonychia  mytilus:  This  large  Hypotrichan  is  still  more  favorable 
for  the  study  of  the  movements  of  individuals  under  the  stimulus  of 
heat  or  cold  coming  from  one  side  than  are  the  two  species  of 
Oxytricha.  But  I  have  found  it  less  easy  to  obtain  in  large  numbers, 
and  for  this  reason  have  not  chosen  it  for  the  detailed  description  of 
the  reaction.  Where  comparatively  few  specimens  are  available, 
the  movements  of  individuals  are  easily  studied,  but  there  is  little 
impression  of  any  real  orientation,  such  as  one  gets  clearly  when  large 
numbers  are  used. 

The  movements  of  the  individuals  are  like  those  described  for 
Oxytricha  fallax.  The  animal  in  reacting  always  turns  to  its  right, 
without  regard  to  the  relation  of  this  to  the  direction  from  which  the 
heat  or  cold  is   coming.     With  an   organism    of  the    large   size   of 


REACTIONS    TO    HEAT    AND    COLD.  21 

Stylonychia  this  is  very  evident.  This  turning  to  the  right  under  the 
stimulus  of  heat  and  cold  in  Stylonychia  has  already  been  described 
by  Putter  (1900),  incidentally  to  his  study  of  the  effect  of  contact 
stimuli  in  this  organism. 

Stentor  ccEruleus :  Mendelssohn  includes  in  his  paper  a  note  stat- 
ing that  positive  and  negative  thermotaxis  occur  in  some  species  of 
Stentor,  and  giving  the  optimum  ;  but  he  made  no  study  of  the  mech- 
anism of  the  reactions  in  this  animal.  Had  he  done  so,  it  seems  to  me 
that  he  could  not  have  maintained  his  theory  of  the  way  in  which 
the  reaction  takes  place. 

When  one  end  of  the  trough  is  warmed  the  Stentors  near  that  end 
begin  after  a  few  seconds  to  move  about  more  rapidly.  In  most  cases 
the  movement  is  as  follows :  The  animals  swim  backward  some 
distance,  then  turn  toward  the  right  aboral  side  and  swim  forward 
(the  typical  motor  reaction).  Thus  the  general  effect  is  as  of  an 
irregular  movement  in  all  directions.  Those  individuals  which  swim 
forward  toward  the  other  end  of  the  slide  pass  out  of  the  heated  region  ; 
hence  the  motor  reaction  no  longer  takes  place,  and  the  animals  con- 
tinue to  swim  forward.  Those  which  start  in  any  other  direction  do 
not  escape  from  the  heated  region,  and  therefore  soon  give  again  the 
motor  reaction,  backing  and  turning  again  to  the  right.  Thus  only 
those  that  swim  away  from  the  heated  region  continue  their  course ; 
the  others  are  stopped  and  turned  until  finally  they  too  get  started  in 
the  same  direction.  Therefore,  after  a  period  of  apparently  disordered 
swimming,  there  is  an  evident  orientation  of  many  individuals,  with 
anterior  ends  away  from  the  heated  region.  This  orientation  is  caused 
as  it  were  by  exclusion ;  in  animals  swimming  in  any  direction  but  one 
the  motor  reaction  is  produced,  so  that  only  this  direction  can  be  main- 
tained. After  a  time,  therefore,  a  large  proportion  of  the  individuals 
are  swimming  in  this  direction,  with  a  common  orientation. 

Thus  the  direction  in  which  the  animals  turn  is  determined,  as  in 
the  Hypotricha,  by  the  structure  of  the  body,  and  not  by  the  direction 
from  which  the  heat  comes. 

Those  outside  the  region  where  the  heat  has  reached  the  threshold 
temperature  often  swim  for  some  distance  toward  the  heated  region ; 
then  arriving  at  a  point  where  the  heat  is  effective,  they  give  the  motor 
reaction,  backing  and  turning  to  the  right.  They  are  thus  prevented 
from  entering  the  heated  region. 

If  the  temperature  is  rapidly  raised,  the  animals  may  not  succeed  in 
escaping  from  the  heated  region  until  they  are  injured.  In  this  case 
the  specimen  contracts  strongly  and  swims  backward  a  long  time.  It 
becomes  distorted,  places  the  disk  against  the  bottom  or  other  surface, 
becomes  motionless,  and  finally  dies. 


12  THE    BEHAVIOR   OF   LOWER    ORGANISMS. 

Fixed  specimens  react  less  readily  to  heat  than  do  free-swimming 
specimens.  They  do  not  orient  themselves  with  reference  to  the  direc- 
tion from  which  the  rise  in  temperature  comes.  They  may  remain 
extended  normally,  carrying  on  the  usual  activities,  after  the  tempera- 
ture has  risen  beyond  the  point  which  sets  the  free  specimens  in  rapid 
reaction.  But  as  the  temperature  rises  they  repeatedly  bend  over  into 
a  new  position  (bending  toward  the  right  aboral  side) ,  then  contract 
strongly,  and  finally  free  themselves  from  their  attachment.  There- 
upon they  behave  like  other  free  individuals. 

Spirostomum  ambiguum :  In  this  large  ciliate  the  reactions  to  heat 
and  cold  take  place  in  essentially  the  same  manner  as  is  described 
above  for  Stentor  and  the  Hypotricha,  so  that  it  is  not  necessary  to 
describe  the  phenomena  in  detail.  The  organism  reacts  to  heat  or 
cold  by  backing  and  turning  toward  its  aboral  side  ;  and  this  whether 
the  change  in  temperature  is  uniform  over  the  entire  surface  of  the 
animal  or  whether  it  approaches  from  one  side.  The  movements  of  the 
animal  are  slow,  and  under  the  Braus-Driiner  stereoscopic  microscope 
its  method  of  reaction  is  very  clear.  There  is  little  marked  common 
orientation  at  any  time,  however  ;  this  being  due  to  the  slowness  of  the 
movements  and  the  frequency  of  repetitions  of  the  motor  reaction. 

Bursaria  triincatella :  In  this  very  large  infusorian,  in  which  cer- 
tain differentiations  of  the  body  are  visible  even  to  the  naked  eye,  the 
method  of  reaction  to  heat  and  cold  is  observed  with  the  greatest  ease. 
But  orientation  of  a  large  number  of  individuals  in  a  common  direction 
is  hardly  to  be  noticed,  though  if  Bursaria  could  be  obtained  in  such 
numbers  as  Paramecium  or  Oxytricha,  perhaps  an  indication  of  orien- 
tation would  be  noticeable  in  spite  of  the  slowness  of  movement. 

Bursaria  is  very  inactive,  often  remaining  quiet  for  long  periods. 
It  swims  slowly,  and  frequently  creeps  along  the  bottom  with  ventral 
side  down,  but  may  also  swim  freely  through  the  water,  revolving  to 
the  left.  If  the  temperature  of  the  trough  is  raised  at  one  end,  the 
animals  in  this  region  that  are  moving  freely  through  the  water  swim 
backw^ard,  turn  to  the  right,  and  swim  forward.  This  may  be  repeated 
till  the  organism  passes  out  of  the  heated  region.  Rather  more 
frequently,  however,  the  animal,  after  thus  reacting  once  or  twice,  sinks 
to  the  bottom  and  places  its  ventral  side  against  the  surface.  It  now 
conducts  itself  in  the  same  manner  as  do  the  other  individuals  in  this 
situation,  as  will  be  described. 

The  individuals  which  are  resting  against  the  bottom  (usually  the 
majority  of  those  in  the  trough)  react  as  follows :  They  begin  to  swim 
backward,  keeping  the  ventral  side  down  and  at  the  same  time  circling 
toward  their  own  right  sides.    They  thus  describe  rather  narrow  circles. 


REACTIONS    TO    HEAT    AND    COLD.  23 

This  continues  until  the  heat  becomes  destructive — the  animals  cease 
circling,  become  quiet,  and  finally  disintegrate.  The  reaction  of  those 
individuals  vv^hich  are  resting  or  creeping  on  the  bottom  is  thus  not  of 
a  character  to  save  them  from  destruction. 

Specimens  which  are  by  chance  moving  along  the  bottom  from  a 
cool  region  toward  the  warm  region  do  not  escape ;  they  merely  stop 
and  begin  to  circle  backward  to  the  right  when  they  reach  the  heated 
spot,  and  continue  this  till  they  die. 

Thus  the  reaction  of  Bursaria  to  heat,  while  of  the  same  general 
character  as  that  of  other  infusoria,  must  be  accounted  very  imperfect, 
since  it  hardly  results  in  orientation  at  all,  and  does  not  preserve  the 
animals  from  destruction. 

Paratnecium  caudatum :  *  In  the  second  of  my  studies  (Jennings, 
1899,  pp.  334-336)  I  gave  a  brief  account  of  the  way  in  which,  ac- 
cording to  my  observations,  Paramecium  reacts  to  heat  and  cold. 
From  my  more  recent  studies  I  can  confirm  this  account.  But  as 
Mendelssohn  has  recently  come  to  different  conclusions  for  the  tempera- 
ture reaction  of  this  animal,  and  as  he  misunderstands  certain  points 
in  my  brief  description,  it  seems  desirable  that  I  should  supplement  the 
account  previously  given  in  order  to  make  it  clear. 

Paramecium  reacts  to  heat  and  cold  in  essentially  the  same  manner 
as  is  described  above  in  detail  for  Oxytricha.  When  the  higher  or 
the  lower  temperature  advances  from  one  side  the  animals  swim 
backward,  turn  toward  the  aboral  side,  and  swim  forward  again. 
They  continue  this  until  the  movement  brings  them  into  a  region  of 
more  moderate  temperature.  Paramecium  reacts  more  readily  than 
Oxytricha,  the  reactions  are  repeated  at  shorter  intervals,  and  the 
movements  are  more  rapid,  so  that  a  common  orientation  of  many 
individuals  swimming  away  from  the  region  of  higher  or  lower  tem- 
perature is  more  quickly  produced  and  is  more  striking  to  the  eye.  It 
results  farther  from  this  more  rapid  movement,  as  well  as  from  certain 
other  factors,  that  the  method  of  reaction  in  Paramecium  is  much  less 
easily  observed  than  in  any  of  the  other  infusoria  described.  Indeed, 
Paramecium  is  one  of  the  most  unfavorable  forms  obtainable  for  a 
study  of  reaction  methods,  and  it  is,  I  believe,  due  largely  to  the  fact 
that  this  animal  is  usually  employed  for  such  study  that  progress  has 

♦The  common  Paramecium,  which  appears  everywhere  in  immense  numbers 
in  decaying  vegetation,  receives  from  different  authors  sometimes  the  name 
Paramecium  aurelta^  used  by  Mendelssohn ;  sometimes  the  name  given  above. 
I  use  the  name  caudatum  because  it  appears  to  me  to  be  the  correct  one,  but 
there  is  no  reason  for  considering  the  animals  thus  differently  denominated  to 
be  really  different. 


34  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

been  so  slow  in  appreciating  the  real  nature  of  the  reactions  of  the  in- 
fusoria. If  Stylonychia  or  Oxytricha  or  any  other  of  the  Hypotricha 
had  been  taken  as  the  usual  type  for  study  on  reactions,  many  of  the 
theories  now  maintained  could  never  have  been  put  forth.  The  body 
of  Paramecium  is  comparatively  little  differentiated,  so  that  it  is  diffi- 
cult to  distinguish  oral  and  aboral  sides,  and,  to  multiply  this  difficulty 
many  times,  the  animal  revolves  rapidly  on  its  long  axis,  so  that  oral 
and  aboral  sides  never  retain  for  two  successive  instants  the  same 
position.  It  is  not  wonderful,  therefore,  that  the  method  of  reaction 
by  turning  toward  the  aboral  side  was  not  observed  in  the  first  investi- 
gations on  Paramecium  and  that  many  still  find  it  difficult  to  observe. 
Nevertheless,  it  was  on  Paramecium  itself  that  this  reaction  method  was 
first  observed  (Jennings,  1899),  and  its  existence  was  confirmed  later 
on  the  organisms  where  its  observation  presents  no  difficulties.  Aside 
from  the  direct  observations  of  the  method  of  reaction,  the  following 
facts  throw  light  on  the  way  in  which  the  collections  take  place. 

As  described  in  the  second  of  my  studies 
(Jennings,  1899,  pp.  314,  315),  the  collect- 
ing of  Paramecia  in  regions  of  optimum 
temperature  may  be  produced  in  the  follow- 
ing manner  :  The  infusoria  are  mounted  in 
^  water  which  is  above  the  optimum  temper- 

ature (say  30°)  on  a  slide  beneath  a  cover 
glass  supported  at  its  ends  by  glass  rods.  Into  this  slide  is  introduced 
with  the  capillary  pipette  a  little  cooler  water  (say  at  24°),  which 
covers  a  small  circular  area  in  the  center  of  the  slide.  Very  soon  the 
Paramecia  have  collected  in  this  region  till  a  dense  group  is  formed. 
The  same  result  may  be  obtained  by  placing  a  drop  of  ice  water  on  the 
top  of  the  cover  glass  of  a  slide  of  Paramecia  which  has  been  warmed 
considerably  above  the  optimum  temperature.     (Fig.  9.) 

Are  these  collections  due  to  the  orienting  of  Paramecium  by  the 
heat,  as  maintained  by  Mendelssohn  for  thermotaxis  in  general.?  Ob- 
servation shows  that  they  are  not ;  that  on  the  contrary  the  Paramecia 
gather  in  the  optimum  region  in  the  same  manner  as  they  gather  in  a 
drop  of  weak  acid,  as  described  in  my  studies.  The  Paramecia  on  the 
heated  slide  are  swimming  rapidly  in  all  directions.  They  do  not 
change  their  course  or  become  oriented  in  the  least  when  a  spot  in  a 
certain  part  of  the  slide  is  cooled.     But  as  a   consequence    of  their 


*FiG.  9. — Collection  of  Paramecia  due  to  the  reaction  to  temperature  change. 
The  slide  rests  on  a  vessel  of  water  at  a  temperature  of  45"^.  An  elongated  drop 
of  ice  water  is  placed  on  the  upper  surface  of  the  cover  glass.  The  Paramecia 
quickly  collect  beneath  the  drop  of  ice  water. 


REACTIONS    TO    HEAT    AND    COLD.  25 

rapid  movements  many  of  them  by  chance  enter  the  cooler  region. 
They  do  not  react  at  all  as  they  enter,  but  continue  across.  On 
coming  to  the  other  side  of  the  drop,  however,  they  do  react,  by  back- 
ing and  turning  toward  one  side  (the  aboral).  They  react  whenever 
they  come  to  the  boundary  of  the  cooled  region ;  hence  they  do  not 
leave  it.  In  every  respect  their  behavior  is  like  that  seen  when  Para- 
mecia  collect  in  a  drop  of  weak  acid,  and  I  believe  there  is  no  longer 
anyone  who  holds  to  the  orientation  theory  for  the  gathering  of  Para- 
mecium in  chemicals. 

As  in  the  case  of  chemicals,  it  may  be  demonstrated  to  the  eye  in  the 
following  manner  that  the  method  above  described  suffices  to  account 
for  the  gatherings.  On  the  upper  surface  of  the  cover  glass  is  marked 
a  small  ring  in  ink.  By  confining  the  attention  to  this  ring  it  is  easily 
seen  that  in  the  heated  preparation  of  Paramecia  many  individuals 
cross  the  ring  every  instant,  so  that,  if  these  could  all  be  stopped  in 
the  ring,  a  dense  aggregation  would  soon  result.  Then  the  region 
within  the  ring  is  cooled  by  placing  a  drop  of  ice  water  on  the  cover 
above  it.  The  Paramecia  continue  to  swim  just  as  before,  save  that 
they  no  longer  pass  out  of  the  ring  after  swimming  in,  as  they  did  at 
first.     In  this  way  a  dense  collection  is  soon  formed. 

Mendelssohn  (1902,  ^,  p.  487)  finds  it  inexplicable  w^hy  the  Para- 
mecia should  form  dense  aggregations  at  the  optimum  temperature. 
He  says  that  they  execute  "  only  some  insignificant  movements  "  in 
this  region,  not  swimming  away.  On  the  theory  of  thermotaxis  held 
by  Mendelssohn  this  is  perhaps  inexplicable,  but  this,  it  seems  to  me, 
is  only  because  the  theory  is  incorrect.  Such  collections  are  due  to 
precisely  the  same  factors  as  the  rest  of  the  reaction  to  heat  and  cold 
and  are  clearly  intelligible  when  the  nature  of  the  reaction,  as  described 
above,  is  taken  into  consideration.* 

In  a  former  paper  (Jennings,  1S99,  p.  336),  after  giving  a  brief 
account  of  the  reaction  method  above  described,  I  pointed  out  that  this 
method  does  not  demand  a  sensitiveness  to  such  minute  differences  in 
temperature  as  does  Mendelssohn's  theory,  and  that  therefore  the  sensi- 
tiveness  to   temperature    differences    may   have   been   overestimated. 


*  Mendelssohn  (1902,  b,  p.  487)  supposes  that  I  would  explain  these  gatherings 
at  the  optimum  temperature  through  the  collection  of  Paramecia  in  CO 3  pro- 
duced by  themselves,  and  shows  that  this  would  not  account  for  the  phenomena 
observed  in  these  cases,  though  he  confirms  the  fact  of  the  collections  in  COg. 
But  I  have  by  no  means  maintained  that  such  collections  can  be  produced  only 
by  COg  ;  on  the  contrary,  I  have  given  an  account  of  many  different  agencies 
that  will  give  rise  to  such  collections,  and  have  especially  described  the  fact  that 
collections  are  formed  in  a  warmed  region  through  exactly  the  same  reaction  by 
which  they  are  formed  in  CO^.     (Jennings,  1899,  P*  S^SO 


26  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Mendelssohn  (1902,  a,  p.  406)  misunderstands  my  ground  for  this 
statement.  He  supposes  that  I  hold  that  the  Paramecia  do  not  react 
to  differences  in  temperature  less  than  that  existing  in  a  certain  illus- 
trative experiment,  where  one  end  of  the  slide  was  resting  on  ice,  while 
the  other  was  heated  to  40°.  This  experiment  was  purely  for  the 
purpose  of  bringing  the  phenomena  of  thermotaxis  concretely  before 
the  attention  of  the  reader ;  its  details  had  no  special  significance.  I 
have  not  the  slightest  reason  for  doubting  the  entire  accuracy  of  the 
quantitative  experimental  results  set  forth  by  Mendelssohn,  and  consider 
them  a  most  valuable  addition  to  our  stock  of  exact  data.  But  the 
calculation  of  the  sensitiveness  of  the  organisms  concerned,  from  these 
experimental  results,  involves  a  certain  interpretation  as  to  the  reaction 
method,  and  it  was  this  interpretation  that  I  called  in  question.  Men- 
delssohn, in  accordance  with  his  general  theory,  holds  that  the  reaction 
is  due  to  the  difference  in  temperature  between  the  two 
ends  of  the  organism,  and  he  calculates  that  this  difference 
in  temperature  could  amount,  in  the  case  of  Paramecia, 
to  but  0.01°  C.  According  to  the  reaction  method  which 
I  have  described  above,  however,  it  is  not  the  difference 
in  temperature  between  the  two  ends  of  the  same  indi- 
vidual that  causes  the  reaction.  Consider  a  slide  cooled 
below  the  optimum  at  the  end  a  ;  above  the  optimum  at 
the  end  b  (Fig.  10),  the  optimum  temperature  for  the 
Paramecia  being  between  the  lines  x  and  y.  The  animal 
p  ^        may  swim  a'  considerable  distance  from  a  position  y^  at 

one  side  of  the  optimum,  to  a  position  a?,  at  the  other  side 
of  the  optimum,  before  it  reacts  (by  backing  and  turning,  etc.)  at  all. 
We  have  no  ground  for  maintaining  then  that  it  perceives  any  less  differ- 
erences  in  temperature  than  that  between  the  lines  x  and  jv,  and  this 
difference  will  be  much  greater  than  that  between  the  two  ends  of  the 
animal.  A  similar  diagram  could  be  made  for  the  case  where  the  tem- 
perature is  raised  or  lowered  only  at  one  end  of  the  slide.  It  seems  to 
me  correct,  therefore,  that  the  sensitiveness  to  temperature  differences 
has  probably  been  much  overestimated.  The  only  way  that  it  could 
be  estimated  would  be  by  observation  of  individuals  to  determine  the 
extent  of  the  stretch  x-y  over  which  they  pass  before  reacting,  and  to 
calculate  the  difference  in  temperature  between  the  ends  of  this  stretch. 
It  would  of  course  be  very  diflScult  to  do  this  with  accuracy. 

Mendelssohn's  view  that  it  is  the  difference  in  temperature  between 
the  two  ends  of  the  same  individual  that  determines  the  reaction  is  not 


*  Fig.  10. — Diagram  illustrating  conditions  necessary  for  determining  the  sen- 
sitiveness  of  Paramecia  to  differences  in  temperature.     See  text. 


REACTIONS    TO    HEAT    AND    COLD.  27 

only  rendered  inadmissible  by  the  reaction  method  above  described, 
but  it  is  rendered  a  priori  improbable  by  certain  other  considerations. 
First  we  have  the  fact  that  the  anterior  end  is  much  more  sensitive  than 
the  posterior.  Of  course  it  is  impossible  to  measure  this  difference  in 
sensitiveness,  yet  the  experiments  with  mechanical  and  chemical  stimuli 
show  that  it  is  great.  In  many  infusoria,  while  the  slightest  touch  at 
the  anterior  end  causes  a  pronounced  reaction,  it  requires  a  strong  stroke 
at  the  posterior  end  to  produce  even  a  slight  reaction.  (See  Jennings, 
1900,  pp.  238,  243,  251.)  Owing  to  the  much  greater  sensitiveness  of 
the  anterior  end,  it  is  probable  that,  with  the  posterior  end  but  0.01° 
warmer  than  the  anterior,  the  reaction,  if  any,  would  be  due  to  the  tem- 
perature of  the  anterior  end.  In  other  words,  there  is  reason  to  suppose 
that  the  threshold  temperature  for  the  anterior  end  would  be  considera- 
bl)'  lower  than  that  for  the  posterior  end.  If  this  is  true  the  usual  tem- 
perature reactions  would  be  throughout  due  primarily  to  stimulation 
at  the  anterior  end  ;  and  the  reaction,  as  we  have  seen,  is  of  just  the 
character  which  would  be  expected  from  this.  The  first  stage  in 
the  reaction  is  to  swim  backward^  and  this  is  true  also  when  the  animal 
is  dropped  directly  into  water  of  uniformly  high  or  low  temperature,  so 
that  the  temperature  of  the  anterior  end  is  no  greater  than  that  of  the 
posterior  end.  There  is  no  explanation  for  the  swimming  backward 
under  these  circumstances  on  the  theory  that  accounts  for  thermotaxis 
by  the  different  temperature  of  the  two  ends. 

A  second  factor  which  must  be  taken  into  consideration  relates  to  the 
currents  produced  by  the  cilia  of  the  organism  itself.  As  shown  above 
(p.  13) ,  the  water  of  a  higher  temperature  (supposing  that  we  are  deal- 
ing with  the  reaction  to  heat) ,  would  as  a  rule  first  reach  the  anterior 
end  and  pass  at  once  down  the  oral  groove,  on  the  oral  side  (Fig.  6) . 
The  natural  result  therefore  would  be  a  turning  toward  the  opposite  or 
aboral  side,  and  this  is  exactly  what  we  find  takes  place.  We  should 
therefore  not  expect  the  organism  to  turn  directly  away  from  that  end 
of  the  trough  from  which  the  heat  comes,  for  the  heated  water  may  not 
reach  the  Paramecium  from  that  side  at  all. 

As  will  be  seen,  the  facts  adduced  in  the  last  paragraph  are  not  incon- 
sistent with  the  idea  that  the  organism  turns  directly  away  from  the 
side  stimulated.  It  is  the  oral  side  which  is,  as  a  rule,  stimulated,  and 
the  organism  turns  toward  the  aboral  side.  We  seem  thus  to  obtain 
a  most  gratifying  union  of  two  apparently  opposed  views.  But  the 
reactions  to  certain  other  stimuli  do  not  admit  of  such  a  union.  This 
is  notably  true  of  the  reactions  to  mechanical  stimuli,  as  shown  in  a 
previous  paper  (Jennings,  1900),  and  of  the  reactions  to  light,  to  be 
described  in  the  following  paper. 


28  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

SUMMARY. 

The  ciliate  infusoria  react  in  the  same  manner  to  heat  and  cold  as 
to  most  other  classes  of  stimuli ;  the  response  on  coming  into  a  region 
where  the  temperature  is  above  or  below  the  optimum  is  by  backing 
and  turning  toward  a  structurally  defined  side,  followed  by  a  movement 
forward.  This  reaction  is  repeated  as  long  as  an  effective  supraoptimal 
or  suboptimal  temperature  continues.  The  result  is  to  prevent  the 
organisms  from  entering  regions  of  marked  supraoptimal  or  suboptimal 
temperature,  and  to  cause  them  to  form  collections  in  regions  of  opti- 
mal temperature.  The  common  orientation  of  a  large  number  of 
individuals  sometimes  produced  in  this  way  is  an  indirect  result  of  the 
method  of  reaction.  Since  movement  in  any  other  direction  than  a 
certain  one  is  stopped,  the  organisms  after  many  trials  come  into  this 
direction.  Orientation  is  therefore  by  "  exclusion,"  or  by  the  method 
of  trial  and  error.  In  many  of  the  organisms  orientation  is  not  a 
noticeable  feature  of  the  reaction. 


SECOND    PAPER 


REACTIONS  TO  LIGHT  IN  CILIATES 
AND  FLAGELLATES. 


29 


REACTIONS  TO  LIGHT  IN  CILIATES  AND 

FLAGELLATES.  ^ 


In  the  reactions  to  light  we  are  dealing  with  a  stimulating  agent 
which  differs  in  one  very  important  respect  from  chemicals  and  from 
heat  or  cold.  The  distribution  of  the  agent  with  which  we  are  con- 
cerned is  not  affected  by  the  currents  of  water  produced  by  the  organism  ; 
hence  there  is  no  tendency  for  one  side  or  part  of  the  organism  to  be 
more  strongly  affected  than  the  rest,  as  was  found  to  be  the  case  for 
chemicals  and  for  heat  and  cold.  This  peculiarity  light  shares  with 
the  electric  current  and  with  radiant  heat.  The  conditions  demanded 
for  immediate  orientation  through  direct  action  of  the  agent  on  the 
locomotor  organs,  in  the  manner  required  by  the  general  theory  of 
tropisms  as  set  forth  in  the  foregoing  paper  (p.  7),  are  therefore  present. 
In  a  recent  paper  Holt  &  Lee  (1901)  have  attempted  to  show  that 
the  reactions  of  organisms  to  light  actually  take  place  in  accordance 
with  this  theory. 

We  shall  examine  the  reactions  to  light  in  Stentor  ccerul^us  and  in 
certain  flagellates,  in  order  to  determine  whether  they  take  place  in 
accordance  with  the  tropism  schema,  and,  if  not,  just  how  they  do  occur 
and  on  what  factors  they  depend. 

THE  CILIATA. 
STENTOR  C^RULEUS. 

As  is  well  known,  very  few  of  the  ciliate  infusoria  react  to  light. 
Light  reactions  have  been  described  by  Engelmann  (1882,  a)  for  several 
chlorophyllaceous  ciliates  ;  by  Verworn  (18S9,  Nachschrift)  for  Pleuro- 
ncma  chrysalis;  and  by  Davenport  (1897)  ^"^  Holt  &  Lee  (1901)  for 
Stentor  cceruleus.  In  none  of  the  ciliates  have  the  reactions  been 
described  in  sufficient  detail  to  enable  us  to  determine  their  exact 
nature. 

In  Stentor  cceruleus  the  reaction  to  light  manifests  itself  in  the 
culture  dish  by  the  usual  aggregation  of  the  organisms  at  the  side  away 
from  the  window.  If  a  number  of  Stentors  are  removed  to  a  watch 
glass  or  trough,  and  this  is  placed  near  a  window  or  other  source  of 
light,  most  of  the  Stentors  are  soon  found  on  the  side  of  the  vessel  away 
from  the  light.     If  one-half  of  the  glass  is  shaded  by  a  screen,  most  of 

31 


32  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

the  Stentors  are  soon  found  in  the  shaded  half.  6".  ccEruleus  thus  shows 
the  phenomenon  usually  called  negative  phototaxis. 

It  is  to  be  noted  that  not  all  the  Stentors  are  to  be  found  on  the  side 
away  from  the  light,  or  in  the  shaded  half  of  the  vessel.  On  the  con- 
trary, a  considerable  fraction  of  the  whole  number  will  usually  be  found 
swimming  about  in  all  parts  of  the  dish,  or  at  rest  in  the  lighted  portion. 
The  light  reaction  is  thus  somewhat  inconstant,  and  varies  among 
different  individuals.  It  varies  considerably  with  Stentors  of  different 
cultures ;  from  some  cultures  almost  all  the  individuals  show  it,  while 
from  others  it  is  barely  noticeable.  This  variability  and  inconstancy 
run  through  all  manifestations  of  the  light  reaction  in  Stentor. 

A  word  further  needs  to  be  said  as  to  the  behavior  of  individuals 
which  are  not  free-swimming,  but  are  fixed  by  the  posterior  end.  Such 
individuals  do  not  react  at  all  to  light.  When  light  is  thrown  on  them 
they  remain  in  the  positions  in  which  they  are  found  at  the  beginning, 
neither  contracting  nor  in  any  way  changing  their  position.  No  matter 
whether  the  light  is  weak  or  strong,  and  without  regard  to  the  direction 
from  which  it  comes,  fixed  Stentors  give  no  reaction  and  show  no 
orientation  with  reference  to  light.  The  contact  reaction  apparently 
inhibits  the  light  reaction  completely.  We  shall  therefore  omit  the 
fixed  individuals  from  consideration  in  the  remainder  of  the  account, 
confining  attention  to  the  free-swimming  specimens. 

The  typical  motor  reaction  of  Stentor,  by  which  it  responds  to  most 
stimuli,  is  as  follows:  The  Stentor  stops  or  swims  backward  a  short 
distance,  then  turns  toward  the  right  aboral  side,  and  resumes  its  for- 
ward motion.  This  is  the  reaction  which  is  produced  by  strong 
mechanical  stimuli,  by  heat,  and  by  chemical  stimuli,  acting  upon  the 
anterior  end  or  upon  the  body  as  a  whole. 

How  is  the  reaction  to  light  brought  about  .'^  To  answer  this  ques- 
tion it  is  best  to  arrange  experiments  in  such  a  way  as  to  distinguish 
as  far  as  possible  the  effect  due  to  unequal  illumination  of  different 
areas  from  the  effect  due  to  the  direction  from  which  the  light  is  coming. 

In  order  to  produce  strong  differences  in  illumination  in  different 
areas  of  the  space  in  which  the  Stentors  are  found,  a  flat-bottomed 
glass  vessel  containing  many  Stentors  in  a  shallow  layer  of  water  was 
placed  on  the  stage  of  the  microscope,  in  a  dark  room.  From  beneath 
strong  light  was  sent  upward  through  the  opening  of  the  diaphragm, 
by  throwing  the  light  from  the  projection  lantern  (using  the  electric 
arc  light)  on  the  substage  mirror.  By  this  the  light  was  directed  up- 
ward through  the  vessel  containing  the  Stentors.  Thus  a  small, 
definitely  bounded  circular  area  was  illuminated,  while  the  rest  of  the 
vessel  remained  in  darkness.  A  black  screen  was  usually  placed  over 
the  diaphragm  opening  of  the  microscope  in  such  a  way  as  to  shade  one- 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


33 


half  of  the  circular  area,  making  a  sharp  line  (x-y,  Fig.  1 1)  dividing  the 
light  from  the  darkness.  A  mirror  was  placed  above  the  microscope, 
inclined  in  such  a  position  as  to  project  the  image  of  the  Stentors,  very 
much  magnified,  on  the  ordinary  vertical  screen  used  for  receiving 
lantern  slide  viev^s.  Thus  the  behavior  of  the  Stentors  could  be  studied 
with  great  ease  on  the  screen. 

The  heat  from  the  lantern  was  cut  out,  so  far  as  possible,  by  placing 
between  it  and  the  mirror  of  the  microscope  a  glass  cell  three  inches 
thick,  filled  with  cold  water.  In  this  manner  the  heat  was  excluded  to 
such  an  extent  as  to  fall  below  the  threshold  for  the  stimulation  of 
Stentor  by  heat.  This  was  demonstrated  by  comparing  the  reactions 
of  Stentor  with  those  of  Paramecium.  Stentor  is  less  sensitive  to 
changes  in  temperature  than  is  Paramecium  ;  this  was  clear  in  my  ex- 
periments on  the  reaction  to  heat.  Par- 
amecium does  not  react  at  all  on  passing 
into  the  area  illuminated  by  the  lantern, 
but  swims  about  indifferently  in  both  the 
dark  and  the  light  parts  of  the  dish,  show- 
ing that  the  heat  produced  is  below  the 
threshold  for  Paramecium  ;  it  must  then 
be  below  the  threshold  for  Stentor. 

The  free  Stentors  in  the  unlighted  part 
of  the  vessel  swim  about  at  random. 
Many  individuals  thus  come  by  chance  to 
the  line  x-y,  Fig.  1 1 ,  where  they  would 
pass  into  the  lighted  area.  These  at 
once  back  a  little,  then  turn  toward  the 
right   aboral    side,   and    swim   forward 

again.  The  turning  toward  the  right  aboral  side  is  usually  through  an 
angle  sufficient  to  direct  the  Stentor  away  from  the  lighted  area  (see 
I,  2,  3,  4,  Fig.  ii)  ;  if  it  is  not,  the  Stentor  repeats  the  reaction  until, 
after  one  or  two  trials,  it  swims  into  the  unlighted  region. 

Many  of  the  individuals  react  as  soon  as  the  anterior  end  reaches  the 
lighted  area,  so  that  less  than  one-fourth  of  the  body  is  in  the  light. 
This  shows  that  light  falling  upon  the  anterior  end  alone  is  sufficient 
to  cause  the  reaction. 

A  few  specimens  swim  completely  into  the  lighted  area,  then  react 


♦Fig.  II. — Method  of  studying  the  manner  in  which  Stentor  reacts  to  light. 
The  figure  shows  a  circular  area,  illuminated  from  below,  with  the  light  cut  oft 
from  the  left  side  hy  a  dark  screen,  the  line  x-y  separating  the  light  from  the 
dark  area.  The  Stentors  collect  in  the  dark  area.  The  reaction  of  a  specimen 
which  comes  to  the  line  x-y  is  shown  at  i,  2,  3,  4. 


34  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

in  the  manner  above  described.  In  such  cases  the  nature  of  the  reac- 
tion is  seen  with  especial  clearness,  the  entire  animal  being  projected 
on  the  screen  and  the  differentiations  of  bodily  structure  (mouth,  oral 
and  aboral  sides,  etc.)  being  conspicuous.  Specimens  which  swim 
completely  into  the  lighted  area  are  usually  compelled  to  react  two  or 
more  times  before  they  escape  from  the  lighted  region. 

When  the  light  is  cut  off  entirely  the  Stentors  distribute  themselves 
throughout  the  dish.  If  the  light  is  now  admitted  from  below,  the 
unattached  Stentors  in  the  lighted  area  react  by  swimming  backwards 
a  certain  distance,  turning  toward  the  right  aboral  side,  then  swimming 
forward  again.  This  reaction  is  repeated  frequently  until  after  an 
interval  the  Stentors  are  carried  by  these  movements  outside  the  lighted 
area.  They  then  cease  to  give  the  reaction.  The  reaction,  under  these 
conditions,  is  thus  the  same  as  that  produced  when  Stentors  or  Para- 
mecia  are  subjected  to  other  adequate  stimuli,  as  when  they  are  placed 
in  a  chemical  or  dropped  into  very  warm  or  very  cold  water.  The 
result  of  the  reaction  is,  in  every  case,  to  remove  the  organism  from 
the  sphere  of  action  of  the  stimulus.  When  the  stimulus  is  light  this 
result  is  produced  in  exactly  the  same  way  as  when  the  stimulus  is 
heat  or  cold  or  a  chemical. 

The  same  results  may  be  obtained  by  lighting  the  vessel  containing 
the  Stentors  directly  from  above  and  shading  one  portion  with  a  screen. 
The  Stentors  remain  in  the  shaded  region,  responding  by  the  motor 
reaction  above  described  when  they  come  to  the  lighted  area.  With  a 
favorable  culture  the  experiment  succeeds  even  when  the  source  of 
light  is  comparatively  feeble,  as  when  an  ordinary  incandescent  electric 
light  is  used  as  the  source  of  illumination. 

The  results  so  far  show  that  a  sudden  increase  in  the  intensity  of 
illumination  induces  in  Stentor  a  reaction  which  is  of  the  same 
character  as  the  reaction  to  other  strong  stimuli.  Such  a  sudden 
increase  may  be  due  either  to  the  passage  of  the  Stentor  from  a  dark 
to  a  light  region,  or  to  a  sudden  increase  in  the  brightness  of  the  light 
which  falls  upon  the  animal.  The  general  effect  of  the  reaction  is  to 
prevent  the  Stentor  from  entering  a  brightly  illuminated  area,  or  to 
remove  it  from  such  an  area. 

We  may  now  arrange  the  conditions  so  that  the  light  shall  come 
from  one  side,  while  at  the  same  time  differences  in  illumination  shall 
exist  in  different  regions.  This  may  be  done  by  illuminating  the  vessel 
containing  the  Stentors  from  the  side,  then  covering  one  portion  of  the 
vessel  with  a  screen. 

The  organisms  are  placed  before  a  lighted  window,  or  an  incandes- 
cent electric  light,  in  a  vessel  with  a  plane  front  (Fig.  12).      One-half 


REACTIONS    TO    LIGHT    IN    CII.IATES    AND    FLAGELLATES. 


35 


of  the  vessel  is  then  cut  off  from  the  light  by  a  screen  (5),  the  shadow 
of  which  passes  across  the  middle  of  the  vessel  containing  the  Stentors. 
One  side  of  the  vessel  is  thus  in  the  light,  the  other  in  the  shadow, 
and  these  two  regions  are  separated  by  a  sharp  line  (Fig.  12,  x  y). 

The  Stentors  are  soon  all  collected  in  the  shaded  side  of  the  vessel. 
Here  they  swim  about  freely  in  all  directions,  but  do  not  cross  the  line 
into  the  lighted  portion.  Now,  by  focusing  the  Braus-Driiner  on  this 
line,  the  behavior  of  the  individuals  on  reaching  it  may  be  observed. 

It  is  well  to  examine 

the  conditions  in  this  case     ». 

with  care,  as  they  present 
opportunities  for  a  pre- 
cise and  crucial  test  of 
the  theory  that  the  reac- 
tion to  light  is  due  to  a  di-    -* 

rect  orientation  through 
the  falling  of  light  on  one 
side  of  the  organism  (pho- 
totaxis  or   phototropism 

in  the  strict  sense,  as  de-    *■ 

fined  by  Holt  &  Lee). 
In  the  lighted  portion  of 
the  vessel  the  rays  of  light 
come  from  a  certain  direc- 
tion, as  indicated  by  the  ^ 
large  arrows  (Fig.   12). 

In  the  shaded  region  there     ^ 

is  not  enough  light  to  pro- 
duce orientation,  the  ani- 
mals swimming  in  every  *' 
direction.     On  passing 
from    the  shaded  region 

across  the  line  x-y  into  the  lighted  region,  the  animal  should  (according 
to  the  tropism  theory)  become  oriented.  According  to  the  theory  of 
negative  phototaxis  by  direct  orientation  due  to  differential  action  on 


Fig.  12.* 


♦Fig.  12.— Method  of  testing  the  manner  of  reaction  to  light  in  Stentor.  The 
large  arrows  show  the  direction  from  which  the  light  rays  come.  A  screen  {s) 
cuts  off  the  light  from  half  the  vessel,  leaving  a  line  {x-y)  separating  a  shaded  part 
from  a  lighted  part.  The  Stentors  collect  in  the  shaded  part,  here  swimming 
about  without  orientation.  At  a  (i,  2,  3,  4;  we  see  a  diagram  of  the  reaction 
required  by  the  tropism  schema  when  the  organism  swims  across  the  line  x-y, 
while  at  ^  (i,  2,  3,  4)  we  have  a  diagram  of  the  reaction  as  actually  given  under 
these  conditions. 


36  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

the  two  sides,  the  animals  on  crossing  the  line  should  become  oriented 
by  turning  directly  away  from  the  source  of  light,  as  shown  in  the 
diagram  (Fig.  12)  at  a.  The  animal  would  then  be  expected  to  swim 
in  the  direction  x-y  as  shown  by  the  specimen  «,  i,  2,  3,  4. 

It  cannot  be  held  that  the  real  source  of  light  for  the  Stentors  is  that 
reflected  from  the  bottom  or  sides  of  the  dish  in  the  lighted  region,  and 
hence  coming  on  the  whole  from  a  direction  perpendicular  to  the  line 
xy^  for  the  behavior  of  the  Stentors  shows  that  this  is  not  the  case, 
A  Stentor  in  the  shaded  region,  close  to  the  line  x-y^  as  at  c,  Fig.  12, 
receives  whatever  light  there  may  be  thus  reflected  exactly  as  it  does 
after  it  has  crossed  the  line,  yet  it  shows  no  reaction  and  does  not 
orient  itself  in  any  way.  On  the  other  hand,  as  soon  as  it  crosses  the 
line  x-y^  so  as  to  receive  the  light  coming  from  the  window,  it  reacts 
strongly,  as  we  shall  see.  It  is  thus  clearly  the  light  from  the  window, 
coming  in  the  direction  shown  by  the  large  arrows,  that  causes  the  re- 
action ;  hence  the  Stentor  ought,  according  to  the  direct  orientation 
theory,  to  orient  itself  in  the  line  of  these  rays. 

When  a  Stentor,  swimming  at  random,  reaches  the  line  x-y^  it 
reacts  by  stopping  suddenly,  then  turning  toward  its  aboral  side, 
then  swimming  forward.  It  thus  swims  about  until  its  anterior  end  is 
again  within  the  shadow,  where  it  continues  to  swim  forward  (Fig.  12, 
3,  I,  2,  3,  4).  Often  the  first  reaction  is  not  sufficient  to  direct  it  into 
the  shadow  ;  in  this  case  the  reaction  is  repeated  ;  one  to  three  reactions 
almost  invariably  bring  the  Stentor  back  into  the  shadow.  It  has  no 
particular  orientation  in  the  shadow,  but  swims  in  whatever  direction 
it  happens  to  be  headed. 

Very  frequently  the  animals  react  when  the  anterior  end  alone  has 
crossed  the  line,  so  that  less  than  the  anterior  half  of  the  body  is  lighted. 
In  other  cases  the  animal  swims  completely  across  the  line,  sometimes 
for  a  distance  greater  than  its  own  length,  into  the  light,  before  it  reacts. 
In  any  case  the  reaction  is  that  above  described. 

Does  the  Stentor,  when  it  turns  on  entering  the  light,  always  turn 
away  from  the  source  of  light,  as  the  theory  of  direct  orientation 
requires  ? 

At  the  moment  of  crossing  the  line  into  the  light  the  Stentor  may 
occupy  various  positions.  It  will  be  well  to  note  specifically  the  re- 
action in  certain  of  these  positions,  as  we  obtain  here  the  observations 
which  furnish  an  exact  and  crucial  test  of  the  direct  orientation  theory. 

I.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed 
toward  the  source  of  light  (Fig  12,  b).  It  therefore  turns  (as  usual) 
toward  its  aboral  side.  It  thus  swings  its  anterior  end  toward  the 
source  of  lights  in  the  direction  opposite  that  required  by  the  direct 


REACTIONS   TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


37 


orientation  theory.  This  observation  was  made  repeatedly  in  a  very 
large  number  of  cases  ;  not  a  single  exception  to  it  was  observed.  The 
swinging  of  the  anterior  end  is  continued  past  the  point  where  the  light 
falls  directly  upon  it  until  the  animal  is  directed  again  into  the  shadow, 
as  illustrated  in  the  diagram  (Fig.  12,  ^,  i,  3,  3,  4). 

2.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed  away 
from  the  source  of  light.  In  this  case  it  turns  (as  usual)  toward  the 
aboral  side,  thus  swinging  its  anterior  end  away  from  the  source  of  light. 

3.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed 
upward  or  downward  or  in  some  intermediate  position.  In  every  case 
it  turns  toward  the  right  aboral  side,  in  whichever  way  this  is  directed. 


Fig.  13  * 

The  writer  wishes  it  to  be  understood  that  the  foregoing  statements 
as  to  the  direction  in  which  the  animal  turns  are  presented,  not  merely 
as  interpretations  in  accordance  with  a  certain  theory,  but  as  direct, 
unequivocal  observations,  many  times  repeated.  Thus,  on  passing  from 
a  darker  to  a  lighter  area,  even  when  the  light  comes  from  one  side, 
the  Stentors  react  merely  to  the  difference  in  illumination,  without 
regard  to  the  direction  from  which  the  light  comes.  The  direction  of 
turning  is  determined  throughout  by  an  internal  factor,  not  by  the  side 
of  the  animal  on  which  the  light  falls,  nor  by  the  direction  of  the  rays  of 
light.     We  have  put  the  theory  of  orientation  by  direct  differential 


♦Fig.  13. — Another  method  of  testing  the  manner  in  which  Stentor  reacts  to 
light.  For  a  side  view  of  this  apparatus,  see  Fig.  14.  Light  comes  from  the 
left  side,  in  the  direction  indicated  by  the  arrows.  A  screen  (5)  is  interposed 
between  the  source  of  light  and  the  vessel  containing  the  Stentors.  This  screen 
is  of  such  a  height  (as  illustrated  in  Fig.  14)  that  it  cuts  off  the  light  from  the 
half  (/I)  of  the  vessel  next  to  the  window,  leaving  the  other  half  {B)  lighted. 
At  c  (I,  2,  3,  4,  5)  is  seen  the  reaction  method  of  a  specimen  which  swims  across 
the  line  x-y,  separating  the  shaded  half  yl  from  the  lighted  half  5. 


3S 


THK  BEHAVIOR  OF  LOWER  ORGANISMS 


action  of  the  light  on  the  two  sides  of  the  animal  to  a  precise  test,  and 
found  it  to  be  incorrect. 

The  same  result  is  brought  out  in  perhaps  a  still  more  striking 
manner  by  the  following  method  of  experimentation :  A  vessel  con- 
taining Stentors  is  placed  on  a  dark  background  near  a  source  of  light 
(a  window  or  an  incandescent  electric  lamp).  The  light  thus  comes 
from  one  side  and  a  little  from  above.  An  opaque  screen  is  placed 
between  the  window  and  the  vessel  containing  the  Stentors,  of  such  a 
size  and  in  such  a  position  that  the  top  of  the  shadow  of  the  screen  falls 
across  the  middle  of  the  vessel  on  the  line  x-y  (Fig.  13  ;  see  also  Fig. 
14).  Thus  the  half  of  the  vessel  next  to  the  window  {A)  is  darker 
than  the  farther  half  {B)^  and  the  Stentors  collect  in  this  shaded  half 
After  some  time  scarcely  a  specimen  is  found  in  the  lighted  part  of  the 
vessel  away  from  the  window.  The  conditions  in  this  case  are  illus- 
trated in  the  side  view  (Fig.  14). 

The  exact  behavior  of  the  Stentors  in 
darkened  portion  of  the  vessel  is  then 
3ied  b}'  focusing  upon  them  the  Braus- 
iner  microscope.     The  Stentors  within 
shaded  area  are  not  oriented  nor  gath- 
ered in  any  particular  region, 
but  swim  about  at  random. 
When  one  of  the  specimens 
comes  in  its  course  to   the 
line  AT-j^  (Fig.  13),  separating 
the  darkened  area  from  the 


Fig.  14.* 


light,  it  responds  to  the  sudden  light  which  falls  upon  it  from  the 
window  by  giving  the  motor  reaction,  turning  to  the  right  aboral  side 
and  swimming  back  into  the  shaded  region.  Often  the  reaction  occurs 
as  soon  as  the  anterior  end  of  the  Stentor  has  crossed  the  line  x-y^  so 
that  the  entire  Stentor  does  not  pass  out  into  the  lighted  area.  In  other 
cases  the  specimen  crosses  the  line  x-y  completely  before  the  reaction 
occurs,  so  that  the  entire  body  is  illuminated.  It  then  reacts  in  the 
usual  manner,  turning  toward  the  right  aboral  side,  so  that  it  is  headed 
toward  the  shaded  region  ;  thus  shimming  back  across  the  line  (Fig. 
13,  c).  After  returning  into  the  shaded  region  the  animals  swim  about 
at  random  as  before. 

What  is  the  reason  for  the  return  of  the  Stentor  into  the  darkened 
area  after  it  has  crossed  the  line  into  the  light  region.? 

*  Fig.  14. — Sectional  view,  from  the  side,  of  the  conditions  shown  in  Fig.  13. 
The  arrows  show  the  direction  of  the  light  rays.  The  region  from  5  to  *  is 
fehaded  by  the  screen  s. 


REACTIONS   TO    LIGHT    IN   CILIATES    AND    FLAGELLATES.  39 

By  SO  doing  it  swims  toward  the  window,  thus  in  the  direction  from 
which  the  strongest  light  is  coming.  According  to  the  theory  of  photo- 
taxis  as  due  to  the  direct  action  of  the  light  on  the  motor  organs  of  the 
animal,  this  movement  is  inexplicable.  Thus,  in  the  analysis  of  this 
theory  given  by  Holt  &  Lee  (1901),  it  is  shown  that  in  the  case  of  a 
negative  organism,  such  as  Stentor,  light  of  supraoptimal  intensity, 
like  that  coming  from  the  window,  must  be  assumed  to  cause  increased 
contraction  of  the  cilia.  After  the  organism  has  passed  across  the  line 
x-y,  or  while  it  is  passing  across  this  line,  it  has  the  anterior  end  directed 
away  from  the  source  of  light ;  according  to  the  tropism  theory  this 
is  a  stable  position  and  should  not  be  changed.  For,  supposing  the 
organism  swerves  a  little  toward  either  side,  the  cilia  on  that  side  will 
be  more  strongly  affected  by  the  light,  so  that  the  animal  will  at  once 
be  turned  back  into  the  position  of  equilibrium  with  anterior  end  directed 
away  from  the  light. 

Nevertheless,  under  these  circumstances  the  organism  does  turn  and 
swim  back  into  the  darkened  area.  An  explanation  for  the  apparent 
movement  of  a  negative  organism  against  the  direction  of  the  light  rays 
is  sometimes  given  in  the  following  form  :  The  light  from  the  window 
is  said  to  fall  upon  the  side  or  end  of  the  dish  farthest  from  the  window 
and  is  reflected  back,  so  that  the  chief  source  of  light  for  the  Stentors 
is  not  the  window,  but  the  side  of  the  dish  opposite  the  window.  The 
animal  therefore  becomes  oriented  with  relation  to  this  source  of  light 
and  swims  away  from  it. 

Comparison  of  the  movements  of  the  Stentors  in  the  darkened  area 
A  with  those  in  the  lighted  area  B  shows  that  this  explanation  can  not 
possibly  be  correct.  Consider  an  individual  at  the  point  3,  Fig.  13, 
which  turns  and  swims  toward  the  window  into  the  dark  region.  It 
is  affected  by  light  from  two  sources,  (i)  from  the  window,  (3)  reflected 
from  the  side  opposite  the  window.  According  to  the  above  theory 
the  turning  is  due  to  the  fact  that  the  light  from  the  opposite  side  is  of 
greater  strength  than  that  from  the  window  (in  itself  a  most  improbable 
suggestion).  Compare  this  Stentor  b  with  an  individual  at  «,  in  the 
darker  region.  This  animal  receives  no  direct  rays  from  the  window, 
yet  does  receive  the  reflected  rays  from  the  opposite  side.  If  these 
reflected  rays  are  sufficient  to  cause  b  to  become  oriented  in  spite  of 
the  opposing  rays  from  the  window,  they  must  produce  the  same  effect, 
a  fortiori^  on  the  individual  a,  since  they  are  the  only  rays  which 
reach  it  Yet  individuals  in  the  position  a  do  not  become  oriented  at 
all.  The  individuals  in  the  shaded  portion  of  the  vessel  swim  about 
in  all  directions,  without  relation  to  the  direction  of  the  light  rays.  It 
is  only  when  they  come  to  the  line  x-y^  where  they  would  pass  into  the 


40  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

region  lighted  directly  from  the  window,  that  they  react  by  turning 
toward  the  right  aboral  side  and  passing  back  into  the  shadow.  It  is 
thus  clear  that  it  is  the  light  corning  from  the  window  to  which  they 
react,  not  the  light  reflected  from  the  sides  of  the  dish.  We  have  here 
realized  the  condition  concerning  which  there  has  been  so  much  dis- 
cussion, and  which  has  been  considered  impossible  and  unrealizable  by 
various  authors — a  negative  organism  reaching  the  darker  region  by 
swimming  toward  the  source  of  strongest  light. 

This  would  of  course  be  quite  inexplicable  on  the  tropism  theory  as 
set  forth  by  Holt  &  Lee.  What  does  it  indicate  as  to  the  real  nature 
of  the  reaction?  To  this  inquiry  there  can  be  but  one  answer.  The 
organism  reacts  on  passing  from  a  darker  to  a  lighter  area,  without 
regard  to  the  direction  from  which  the  light  comes.  It  reacts  to  the 
increase  in  the  amount  of  light  falling  upon  it  as  compared  with  the 
condition  an  instant  before  it  had  passed  into  the  lighted  area.  The 
reaction  takes  the  usual  form — a  backing  and  turning  toward  the  right 
aboral  side,  followed  by  a  forward  motion.  The  organism,  therefore, 
is  directed  again  toward  the  shaded  area,  which  it  enters. 

In  all  our  experiments  thus  far  there  have  been  marked  differences 
in  the  illumination  of  different  areas.  Let  us  now  arrange  the  condi- 
tions so  that  light  comes  from  one  side,  and  all  parts  of  the  vessel  are 
equally  illuminated.  This  may  be  done  by  placing  the  Stentors  in  a 
glass  vessel  with  plane  walls  at  one  side  of  a  source  of  light,  such  as  a 
window  or  the  bulb  of  an  incandescent  electric  light.  The  Stentors, 
after  a  very  short  interval  in  which  the  reaction  seems  indefinite,  swim 
away  from  the  source  of  light,  thus  gathering  at  the  side  away  from 
the  window,  where  they  move  about  in  a  disordered  way.  During  the 
reaction  the  Stentors  are  oriented^  with  the  longitudinal  axis  in  the 
general  direction  of  the  light  rays  and  with  the  anterior  end  away  from 
the  source  of  light. 

Thus  while  it  is  true  that  the  direction  of  the  rays  of  light  has  little 
if  any  effect  on  the  reaction  when  the  animals  are  at  the  same  time 
subjected  to  a  sudden  change  from  dark  to  light,  it  does  determine  the 
direction  of  movement  when  acting  alone.  In  order  to  discover  just 
how  the  reaction  occurs  it  is  necessary  to  observe  the  animals  at  the 
moment  when  they  change  from  their  former  undirected  swimming  to 
the  movement  away  from  the  source  of  light. 

For  determining  this  a  large  number  of  Stentors  are  placed  in  the 
dish  next  the  window  on  a  dark  background.  The  light  comes  from 
one  side  and  a  little  from  above.  The  direct  rays  of  the  sun  were  not 
employed. 

Above  the  glass  vessel  are  focused  the  lenses  of  the  Braus-Driiner 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  41 

Stereoscopic  binocular.  This  gives  a  magnification  of  65  diameters, 
with  a  working  distance  of  3  cm.,  and  permits  exact  observation  of 
the  movements  of  the  individual  Stentors.  To  one  who  has  worked 
only  with  the  monocular  microscope,  the  use  of  the  stereoscopic  binocu- 
lar in  studying  the  movements  of  small  organisms  will  be  a  revelation. 

The  vessel  containing  the  Stentors  is  first  covered  with  a  dark  screen 
and  the  Stentors  are  allowed  to  become  equally  distributed  throughout 
the  dish.  The  screen  is  then  raised,  allowing  the  light  from  the  window 
to  fall  upon  the  Stentors.  Those  which  are  swimming  in  any  other 
direction  than  away  from  the  window  now  turn  and  in  a  short  time 
are  swimming  toward  the  side  of  the  dish  away  from  the  window. 

With  the  Braus-Driiner  the  movements  of  individuals  are  observed 
at  the  moment  of  removing  the  screen.  Some  turn  at  once,  while  most 
continue  for  a  few  seconds  in  the  direction  in  which  they  are  swimming 
and  then  turn.  All  turn  in  every  case  toward  the  right  aboral  side. 
The  turning  is  continued  or  repeated  until  the  anterior  end  is  directed 


ki-_-------i-ii 


Fig.  15.* 

away  from  the  window  ;  then  the  direct  course  is  continued,  carrying  the 
Stentor  to  the  side  of  the  dish  away  from  the  window.  The  direction 
of  turning  is  thus  determined  by  an  internal  factor — the  structure 
of  the  body. 

The  behavior  of  the  Stentors  may  be  controlled  and  studied  more 
exactly  by  a  different  order  of  experimentation.  The  animals  are 
placed  in  a  shallow  rectangular  glass  vessel  on  a  dark  background,  in 
a  room  that  is  entirely  dark  save  for  two  incandescent  electric  lights 
A  and  B  (Fig.  15).  These  are  clamped  in  position,  one  on  each  side 
of  the  dish  containing  the  Stentors,  and  about  eight  inches  from  it. 
Both  these  lights  can  be  turned  on  at  once ;  both  can  be  extinguished 
or  one  can  be  turned  on  while  the  other  is  turned  off.  When  only  one 
is  turned  on  the  direction  of  the  light  can  be  instantly  reversed  by 
simultaneously  extinguishing  this  one  and  turning  on  the  other. 

With  both  lights  extinguished  the  Stentors  in  the  vessel  are  allowed 
to  become  equally  distributed  ;  then  B  is  illuminated.     In  a  short  time 


*FiG.  15. — Method  of  testing  the  reaction  of  Stentor  to  light.     A  and  B  are 
incandescent  electric  lights. 


42  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

most  of  the  individuals  have  gathered  at  the  side  next  to  Ay  as  in 
Fig.  15.  Then  ^  is  extinguished,  while  at  the  same  time  A  is  illumi- 
nated. The  Stentors  then  turn  and  move  toward  B.  They  may  be 
stopped  at  any  point  in  their  course  and  the  direction  of  swimming 
reversed  by  simultaneously  turning  off  one  light  and  turning  on  the 
other.  With  a  sensitive  culture  the  phenomena  take  place  with  con- 
siderable precision,  about  four-fifths  of  the  individuals  responding 
quickly  to  every  reversal  of  the  direction  from  which  the  light  comes. 

Under  these  circumstances  it  is  easy  to  observe  the  individuals  at  the 
moment  of  the  reversal  of  the  course.  The  observation  already  made 
is  confirmed  ;  the  animals  always  turn  at  the  moment  of  reversal  toward 
the  right  aboral  side.  The  reaction  is  thus  of  the  same  sort  that  occurs 
when  there  is  a  sudden  increase  in  illumination.  After  the  first  reaction 
the  anterior  end  is  pointed  in  a  new  direction.  If  this  new  direction 
is  away  from  the  source  of  light  the  animal  swims  forward  in  the 
course  so  laid  out.  If,  as  is  usually  the  case,  the  first  reaction  does 
not  result  in  directing  the  anterior  end  away  from  the  source  of  light, 
the  reaction  is  repeated,  and  this  may  occur  several  times.  Thus  the 
anterior  end  becomes  directed  successively  toward  every  quarter ;  as 
soon  as  it  lies  toward  the  side  opposite  the  light  the  reaction  ceases. 
The  animal  now  swims  straight  ahead  (that  is,  in  a  spiral  with  a 
straight  axis)  away  from  the  source  of  light. 

Thus  while  it  is  clear  that  light  falling  from  one  side  produces  a 
well-defined  orientation,  this  orientation  does  not  take  place  in  such  a 
way  as  to  be  in  accordance  with  the  tropism  theory  as  set  forth,  for 
example,  by  Holt  &  Lee.  It  is  not  the  direct  action  of  the  light  on 
the  motor  organs  of  the  side  on  which  it  impinges  that  determines 
the  direction  of  turning,  but  the  latter  is  due  to  an  internal  factor. 
This  becomes  still  more  evident  when  the  conditions  are  so  arranged 
that  the  direction  of  turning  demanded  by  the  internal  factor  is  the 
opposite  of  that  required  by  the  tropism  theory. 

These  conditions  can  be  fulfilled  in  the  followin'g  manner:  The 
light  to  be  turned  on  (Fig.  15)  is  so  moved  beforehand  that  its  rays 
shall  fall,  not  directly  on  the  anterior  end  of  the  Stentor,  but  obliquely 
at  an  angle  to  the  path  they  are  following.  The  animals  then  react 
as  before,  by  turning  toward  the  right  aboral  side.  It  often  happens 
that  this  involves  first  a  direct  turning  toward  the  light,  as  illustrated 
in  Fig.  16.  In  such  a  case  the  turning  is  continued  or  repeated  until 
the  anterior  end  is  directed^  away  from  the  source  of  light.  We  have 
seen  the  same  result  produced  under  similar  conditions  in  the  experi- 
ments illustrated  in  Fig.  13. 

What  is  the  real  stimulus  to  the  production  of  the  motor  reaction 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


43 


which  results  in  orientation?  The  experiments  directed  precisely 
upon  this  point  show  that  the  stimulus  producing  the  motor  reaction 
is  an  increase  in  the  intensity  of  light  upon  the  sensitive  anterior  end. 
Now,  in  the  reaction  to  a  continuous  light  coming  from  one  side,  the 
conditions  are  present  for  exactly  such  changes  in  the  intensity  of  light 
at  the  anterior  end  as  would  induce  the  observed  reactions.  In  the 
spiral  course  the  animal  swerves  successively  in  many  directions.  In 
certain  directions  the  swerving  subjects  the  anterior  end  to  a  more 
intense  illumination.  This  change  acts  as  a  stimulus  to  produce  the 
motor  reaction,  which  carries  the  anterior  end  elsewhere.  In  other 
directions  the  swerving  leads  to  a  decrease  in  the  intensity  of  light 
affecting  the  anterior  end.  In  this  case  no  reaction  is  produced,  and  the 
organism  continues  to  swim  in  that  general  direction.  The  details  of 
this  method  of  reacting 
will  be  given  in  the  ac- 
count of  the  reactions  of 
Euglena,  where  the  mat- 
ter was  subjected  to  care- 
ful analytical  experimen- 
tation. The  evidence  all 
indicates  that  the  condi- 
tions in  Stentor  are  ex- 
actly parallel  to  those  in 
Euglena. 

We  may  sum  up  our 
results  on  Stentor  as  fol- 
lows :  A  change  from 

dark  to  light,  such  as  is  caused  by  swimming  from  a  shaded  into  an 
illuminated  region,  acts  as  a  stimulus  to  produce  a  typical  motor  reaction  ; 
the  Stentor  backs  and  turns  toward  the  right  aboral  side,  so  that  it 
returns  into  the  shaded  region.  A  change  in  the  illumination  of  the 
anterior  end  produces  the  same  effect  as  a  change  in  the  illumination 
of  the  entire  organism.  The  direction  from  which  the  light  comes  has 
no  observable  effect  on  this  reaction.  But  when  the  illumination  is 
uniform  and  the  light  comes  from  a  definite  direction,  then  light  fall- 
ing on  the  anterior  end  of  the  Stentor  causes  the  reaction,  while  light 
falling  upon  the  posterior  end  causes  none.  The  result  is  that  the 
animal  turns  (toward  the  right  aboral  side)  until  its  anterior  end  is 

*FiG.  i6. — Method  bj  which  Stentor  becomes  oriented  to  light,  when  the  light 
falls  on  the  aboral  side  of  the  animal.  Stentor  turns,  as  shown  by  the  arrows, 
at  first  toward  the  light,  but  the  turning  is  repeated  or  continued  until  the 
anterior  end  is  directed  away  from  the  light 


Fig.  16* 


44 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


directed  away  from  the  source  of  light,  and  swims  in  the  direction  so 
determined.  The  reaction  to  light  is  of  essentially  the  same  character 
as  the  reaction  to  other  usual  stimuli,  and  takes  place  by  what  we  may 
/^  call  the  method  of  trial  and  error.  When  the  animal  comes  to  the 
boundary  of  a  lighted  area,  or  when  the  anterior  end  is  illuminated, 
this  constitutes  error  ;  the  animal  tries  some  other  direction,  and  repeats 
the  trial  till  the  condition  constituting  error  disappears. 

Are  these  results  in  agreement  with  all  the  observed  facts.?  The 
only  point  on  which  perhaps  question  might  arise  is  in  regard  to  the 
production  of  a  clearly  marked  orientation  such  as  we  find  shown  by 
Stentor  when   the   light  falls  upon  it  from  one  side.     In  this  case,  as 


Fig.  17.* 

we  have  seen,  Stentor  swims  directly  away  from  the  source  of  light, 
and  shows  thus  a  typical  orientation.  As  we  have  had  the  dictum 
that  a  motor  reaction,  such  as  I  have  described,  "  cannot  account  for 
an  orientation"  (Garrey,  1900,  p.  313),  it  will  be  well  to  examine  this 
matter  a  little  farther.  In  a  previous  paper  (Jennings,  1900,  a)  I  have 
shown  how  orientation  could  be  produced  through  a  motor  reaction  ; 
the  case  of  Stentor  exactly  realizes  the  possibility  there  set  forth.     If 


♦Fig.  17. — Diagram  to  illustrate  the  difference  between  the  method  of  orienta- 
tion to  light  required  by  the  tropism  schema  and  that  which  actually  takes 
place.  To  light  coming  from  the  direction  shown  by  the  straight  arrows  the 
tropism  schema  requires  that  an  organism  in  the  position  x-y  should  attain  the 
position  y-z  by  turning  in  the  direction  indicated  by  the  ^ broken)  arrow  a-d. 
The  position  is  actually  attained  by  turning  in  the  direction  indicated  by  the 
long  arrow  c-d. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  45 

the  organism  is  at  first  not  oriented  to  lines  of  influence  coming  from  a 
certain  direction,  as  in  Fig.  17,  x-y^  and  then  becomes  oriented,  as  at 
Fig.  17,  J/-Z,  there  are  clearly  more  ways  than  one  by  which  the  orienta- 
tion can  be  produced.  The  essential  question  for  deciding  as  to  the 
nature  of  the  reaction  is  not  whether  orientation  occurs,  but  /zow  the 
orientation  is  brought  about.  This  consideration  has  been  too  often 
lost  sight  of  in  discussions  of  the  behavior  of  the  lower  organisms. 

According  to  the  theory  of  tropisms,  as  defined  by  Verworn,  Loeb, 
and  Holt  &  Lee,  the  orientation  should  be  brought  about  by  the  differ- 
ential action  of  the  external  agent  on  the  different  sides  of  the  organism  ; 
the  organism  should  turn  directly  into  the  line  of  action  of  the  external 
agent,  and  the  direction  of  turning  should  be  determined  by  an  external 
factor,  the  direction  of  the  infalling  rays,  or  the  side  on  which  they 
strike  the  organism.  Now  this  is  a  matter  which  can  be  settled  by 
direct  observation.  Direct  observation  shows  us  in  Stentor  that  orien- 
tation is  not  brought  about  in  the  manner  demanded  by  the  theory. 
The  direction  of  turning  is  determined  by  internal  factors.  The  reac- 
tion which  produces  orientation  is  identical  with  the  typical  reaction 
to  a  mechanical  shock,  to  chemicals,  to  heat  and  cold.  The  difference 
between  what  is  demanded  by  the  theory  of  tropisms  and  what  is 
actually  observed  may  be  made  quickly  evident  to  the  eye  by  Fig.  17. 
According  to  the  theory  of  tropisms  the  orientation  of  a  negatively 
phototactic  organism  should  take  place  by  turning  in  the  direction  of 
the  arrow  a-b ;  in  a  Stentor  in  the  position  shown  (a:-j/),  orientation 
actually  occurs  by  turning  in  the  opposite  direction,  as  shown  by  the 
arrow  c-d. 

The  further  question  then  arises  as  to  why  the  organism  remains 
oriented.  All  the  facts  point,  in  the  case  of  Stentor,  to  the  conclusion 
that  the  reaction  to  a  constant  light  is  due  to  the  intense  illumination 
on  the  sensitive  anterior  end.  As  soon,  therefore,  as  the'anterior  end  is 
turned  away  from  the  light,  as  is  the  case  in  the  position  y-z^  Fig.  17, 
there  is  no  further  cause  for  reaction  ;  the  animal  therefore  remains 
with  its  anterior  end  directed  away  from  the  light ;  that  is,  it  remains 
oriented.  If,  as  a  result  of  reaction  to  some  other  stimulus,  or  in  any 
accidental  manner,  the  animal  comes  into  a  position  such  that  it  is  no 
longer  oriented,  the  ''  motor  reaction"  is  repeated  until  the  animal 
comes  again  into  the  position  of  orientation  in  which  it  is  no  longer 
stimulated. 

How  does  the  method  of  reaction  to  light  here  described  for  Stentor 
agree  with  what  we  know  of  light  reactions  in  other  ciliates.^  As 
noted  in  the  introductory  paragraphs,  comparatively  little  is  known  as 
to  light  reactions   in   this  group  of  organisms.     The  observations  of 


46  THE   BEHAVIOR    OF    LOWER    ORGANISMS. 

Engelmann  (1882,  a)  on  the  light  reactions  of  certain  green  ciliates 
{^Paramecium  bursaria^  Stentor  virldls^  etc.)  were  made  before  the 
typical  motor  reaction — the  turning  toward  a  certain  structurally  de- 
fined side— had  been  observed  in  any  of  the  infusoria.  Engelmann, 
therefore,  paid  no  attention  to  this  point.  Yet  there  is  much  in  his 
account  of  the  reactions  to  light  in  these  organisms  to  suggest  that 
it  takes  place  in  a  way  similar  to  that  which  I  have  described  above 
for  Stentor  cceruleus.  Indeed,  Engelmann's  account,  so  far  as  it 
goes,  fits  precisely  into  the  reaction  method  which  I  have  described 
above.  He  found,  as  I  have,  that  the  organisms  react  either  when  only 
the  anterior  end  is  affected,  or  when  the  entire  organism  is  flooded  with 
light  from  beneath.  The  reaction  consists  in  a  sudden  turn  to  one  side, 
or  a  sudden  start  backward,  just  as  in  Stentor  cceruleus.  The  only 
point  which  is  lacking  in  Engelmann's  account  is  the  observation  as 

to  which  side  the  organism 
11  11  turned  ;  to  this  point  he  did 

^  y  \  \  not  direct  his  attention. 

It  is  interesting  to  note  that 
in  the  account  given  by  Ver- 
worn  (1889,  Nachschrift)  of 
the  reaction  to  light  in  Pleu- 
ronema  chrysalis  there  is 
nothing  tending  to  support 
the  theory  of  an  orienting  tro- 
pism.  According  to  Verworn  the  reaction  of  Pleuronema  to  light  is  by 
a  sudden  leap  ('*  Sprungbewegung"),  which  is  repeated  several  times  if 
the  light  continues.  This  sudden  leap  seems  identical  with  the  "  motor 
reflex"  which  I  have  described  as  the  typical  reaction  to  stimuli  in 
many  ciliates,  and  which  consists  usually  in  a  leap  backward,  followed 
by  a  turning  toward  a  structurally  defined  side.  It  is  in  this  manner, 
as  we  have  seen,  that  Stentor  cceruleus  reacts  to  light  and  the  reac- 
tion, as  in  Pleuronema,  is  often  repeated  many  times. 

Thus  the  other  carefully  studied  accounts  of  reaction  to  light  in  the 
Ciliata,  while  incomplete,  agree  so  far  as  they  go  with  that  which  I 
have  given  for  Stentor,  and  contain  nothing  to  suggest  the  idea  of  an 
orienting  tropism  dependent  upon  unequal  stimulation  of  the  motor 
organs  on  the  opposite  sides  of  the  animal. 


Fig.  18.* 


♦Fig.  18. — Diagram  of  the  reaction  of  Stentor  to  light,  after  Holt  &  Lee. 
Stentors  are  confined  in  a  vessel  behind  a  wedge-shaped  prism  containing  a 
substance  which  partly  cuts  off  the  light,  so  that  one  end  of  the  vessel  is  darker 
than  the  other.  The  usual  course  of  a  Stentor  near  the  lighter  end  is  shown  by 
the  broken  line. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


47 


Davenport's  reference  (Davenport,  1897,  p.  189)  to  the  negative 
light  reaction  of  Stentor  makes  no  attempt  to  explain  the  mechanism  of 
the  reaction.  Holt  &  Lee  (1901)  have  given  an  account  of  some  fea- 
tures of  the  light  reaction  of  Stentor  cceruleus.  They  did  not  attempt 
to  determine  directly  the  mechanism  of  the  reactions,  by  observation 
of  the  exact  movements  of  the  organism.  Specifically,  they  made  no 
observations  to  determine  whether  Stentor  becomes  oriented  by  turn- 
ing directly  away  from  the  source  of  light  or  only  indirectly  through 
a  "  motor  reaction  "  such  as  I  have  described.  They  did  attempt,  how- 
ever, to  show  that  the  gross  phenomena  observed  might  be  interpreted 
in  accordance  with  the  prevailing  theory  of  tropisms  set  forth  on  page 
7  of  the  present  volume.  It  will  be 
well,  therefore,  to  examine  their  obser- 
vations in  order  to  determine  whether 
they  contain  anything  inconsistent  with 
the  account  set  forth  in  the  present 
paper. 

Holt  &  Lee  studied  the  behavior  of 
Stentor  in  an  elongated  trough  which 
was  lighted  from  one  side.  The  light 
passed  through  a  prism  which  con- 
tained a  translucent  fluid  (a  weak  solu- 
tion of  India  ink),  by  means  of  which 
a  portion  of  the  light  was  cut  out  (Figs. 
18  and  19). 

At  the  thicker  end  of  the  prism  more 
light  was  cut  out,  hence  this  end  of  the 
trough  (Fig.  19,  D)  was  darker  than 
the  opposite  end  (Z).  It  was  found 
that  when  Stentors  were  placed  in  the  trough  close  behind  the  prism 
(ato,  Fig.  19)  they  turned  and  swam  away  from*  the  lighted  side  till  the 
back  of  the  trough  was  reached  {a  to  d^  Fig.  19) .  This  is  of  course  ex- 
actly what  happens  when  no  prism  is  interposed.  Reaching  the  back  of 
the  trough  the  animals  give  the  motor  reaction  (by  backing,  then  turning 
toward  the  right  aboral  side),  thus  coming  into  either  the  position  e  or  the 
position^ (Fig.  19).     They  then  swim  forward  again,  strike  the  wall. 


Fig.  19. 


♦Fig.  19.— Reaction  of  such  an  infusorian  as  Stentor  to  light,  under  the  con- 
ditions shown  in  Fig.  18.  After  Holt  &  Lee-  The  animal  in  the  position  x-y^ 
close  behind  the  prism,  turns  and  swims  to  the  position  d^  where  it  comes  against 
the  rear  wall  of  the  trough.  It  then  turns  either  into  the  position  e,  toward  the 
darker  end  Z>,  or  into  the  position/",  toward  the  lighter  end  L.  In  the  latter  case 
it  usually  soon  reacts  again,  and  by  repetition  of  the  reaction  it  finally,  as  a  rule, 
becomes  directed  toward  D.  Thus,  finally,  most  of  the  Stentors  collect  in  the 
dark  end  of  the  trough. 


48  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

and  repeat  the  reaction.  This  is  repeated  many  times  until  the  organ- 
isms are  swimming  either  toward  the  end  D  or  toward  the  end  Z.  In 
course  of  time  it  is  found  that  the  preponderance  of  movement  is  toward 
the  dark  end  Z>,  so  that  the  majority  of  the  Stentors  are  gathered  at  D. 
Why  this  should  be  so  is  explained  by  Holt  &  Lee  as  follows : 

The  reason  whj'  the  Stentors  went  eventually  in  greater  numbers  toward  Z>, 
and  thus  appeared  oftener  to  choose  e  than  /*,  is  that  such  Stentors  as  went  to  e 
progressed  farther  toward  D  than  those  which  went  to/"  could  progress  toward 
L.  These  latter  would  soon  strike  the  wall  a  second  time,  now  pretty  nearly  at 
right  angles,  and  during  the  recoil  the  light  stimuli  would  favor  a  return  to  d. 
It  appears  then  amply  possible  that  the  circumstance  that  the  organism  encoun- 
ters the  wall  of  the  trough  at  an  acute  angle  is  sufficient  to  cause  its  farther 
progress  to  be,  in  the  long  run,  toward  D. 

There  is  evidently  nothing  in  this  account  which  is  inconsistent  with 
the  method  of  light  reaction  which  I  have  described.  On  the  contrary, 
the  reason  why  the  organisms  finally  swim  toward  the  dark  end  and 
gather  there  becomes  much  more  evident  when  the  reaction  method 
that  I  have  described  is  taken  into  consideration.  Let  us  suppose  that 
the  Stentors,  after  striking  the  back  of  the  trough,  turn  in  equal  numbers 
toward  D  and  toward  L,  In  those  swimming  toward  D  the  anterior 
end  is  directed  away  from  the  source  of  strongest  light  (due  to  reflection 
from  the  lighted  end  of  the  dish  Z),  and  the  animals  are  passing  into  a 
region  of  less  intense  light.  There  is  thus  nothing  to  cause  the  ''  motor 
reaction,"  with  its  accompanying  change  in  the  direction  of  movement. 
In  the  Stentors  swimming  toward  Z,  on  the  other  hand,  the  strongest 
light  falls  on  the  anterior  end,  and  the  organisms  are  passing  into  a 
region  of  more  intense  light.  Either  of  these  factors  taken  separately 
may,  as  we  have  seen,  cause  the  motor  reaction  (the  turning  toward 
the  right  aboral  side),  thus  changing  the  direction  in  which  the  Stentors 
swim.  The  animals  which  start  to  swim  toward  Z  will  therefore  soon 
be  turned,  and  only  when  the  direction  of  movement  is  toward  D  will 
there  be  no  cause  for  further  change. 

The  observations  of  Holt  &  Lee  are  thus  quite  in  harmony  with 
the  reaction  method  which  I  have  described,  and  indeed  receive 
illumination  when  this  reaction  method  is  taken  into  consideration. 

In  the  "  fourth  case"  discussed  by  Holt  &  Lee  {loc.  cit.^  pp.  475- 
478),  the  two  factors  mentioned  as  determining  the  turning  of  the 
Stentors  away  from  the  end  Z  would  work  in  opposite  directions  ;  only 
experience  can  tell  which  would  be  more  effective.  As  Holt  &  Lee 
do  not  state  specially  that  they  observed  the  reactions  of  Stentor  under 
these  conditions  no  comment  is  required.  Experiments  of  this  character 
will  be  further  considered  after  we  have  described  reactions  to  light 
in  flagellates. 


REACTIONS    TO    LIGHT    IN    CII.IATES    AND    FLAGELLATES. 


49 


THE  FLAGELLATA. 


In  the  following  pages  we  shall  examine  the  method  of  reaction  to 
light  in  the  flagellates  Euglcna  viridis^  Cryptomonas  i 

ovata^  and  a  species  of  Chlamydomonas. 

EUGLENA  VIRIDIS. 

Euglena  viridis  swims  in  a  spiral  path,  continu- 
ally swerving  toward  that  side  which  bears  the  larger 
"  lip  "  and  the  eye,  the  so-called  dorsal  side  (Fig.  20). 
Its  motor  reaction  to  most  stimuli  is  by  a  sudden  pro- 
nounced turning  toward  the  dorsal  side ;  that  is,  by 
swerving  still  farther  toward  the  same  side  toward 
which  it  swerves  in  its  normal  swimming.  Thus  the 
direction  of  its  path  is  changed  (Jennings,  1900). 

The  general  features  of  the  reaction  of  Euglena  to 
light  have  been  well  worked  out  by  Englemann 
(1882,  a)  and  Wager  (1900).  These  authors  show 
that  Euglena  collects  in  lighted  regions.  The  organ- 
isms pass  into  a  lighted  area  without  reaction.  But 
on  coming  to  the  outer  boundary  of  such  an  area, 
where  they  would  pass  out  into  the  dark,  they  react 
by  turning  round  and  passing  back  into  the  light. 
The  collections  of  Euglense  in  lighted  areas  are  thus 
brought  about  in  much  the  same  manner  as  the  col- 
lections of  Paramecia  in  regions  containing  a  weak 
acid  (Jennings,  1899).  If  diffuse  light  falls  from  one 
side  on  water  containing  Euglenae,  the  organisms  swim 
toward  the  source  of  light.  But  if  strong  sunlight 
falls  upon  them  they  swim  away  from  the  source  of 
light. 

Engelmann  showed  that  the  colorless  anterior  end 
is  the  part  that  is  chiefly  sensitive  to  variations  of  light. 
Often  the  organism  in  a  lighted  area,  on  reaching  the 
edge,  reacts  by  turning  when  only  the  colorless  tip 
has  passed  into  the  darkness. 

The  precise  method  of  reaction  to  light,  the  direc- 
tion of  turning  in  becoming  oriented  or  in  passing 
back  into  the  lighted  area,  was  not  worked  out  by  the  authors  named. 
To  this  point  we  shall  direct  our  attention. 

When  a  large  number  of  Euglenae  are  swimming  toward  the  source 
of  light,  if  the  illumination  is  suddenly  decreased  in  any  way,  they  give 


Fig.  20* 


♦  Fig.  20  shows  the  spiral  path  of  Euglena  in  its  ordinary  swimming. 


50  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

the  typical  motor  reaction  described  in  my  previous  paper  as  a  response 
to  other  classes  of  stimuli  (Jennings,  1900,  p.  235).  That  is,  they 
turn  at  once  toward  the  dorsal  side  (that  bearing  the  larger  lip  and  the 
eye).  This  is  very  easily  seen  when  the  Euglenae  are  mounted  in  the 
ordinary  manner  in  a  thin  layer  of  water  on  a  glass  slide  and  observed 
with  the  microscope  in  the  neighborhood  of  a  window.  If  the  hand 
is  interposed  between  the  slide  and  the  window  all  the  Euglenae  react 
in  the  way  just  described. 

The  reaction  is  a  very  sharp  and  striking  one  and  produces  a  very 
peculiar  impression.  At  first  all  the  Euglenae  are  swimming  in  parallel 
lines  toward  the  window.  As  soon  as  the  shadow  of  the  hand  falls  on 
the  slide  the  regularity  is  destroyed ;  every  Euglena  turns  strongly  and 
may  seem  to  oscillate  from  side  to  side  in  the  manner  described  later. 

The  turning  is  often  preceded  by  a  slight  movement  backward. 
This  was  not  observed  in  the  reactions  to  other  stimuli  (Jennings,  1900, 
p.  235),  though  it  agrees  with  what  we  find  in  most  other  ciliates  and 
flagellates.  In  Euglena  the  reaction  to  variations  in  the  intensity  of 
light  seems  more  sharply  defined  than  to  most  other  stimuli.  The  fact 
that  the  turning  is  always  toward  the  dorsal  side  is  observable  with  the 
greatest  ease.  It  is  particularly  evident  when  the  organisms  are  con- 
fined to  a  thin  layer  of  water,  so  that  they  cannot  swerve  up  or  down, 
but  only  to  the  right  or  left. 

The  reaction  occurs  whenever  the  light  is  suddenly  decreased  in  any 
way.  Certain  different  conditions  under  which  it  occurs  deserve  special 
mention,  (i)  As  we  have  seen,  the  reaction  occurs  when  a  screen  is 
brought  between  the  organisms  and  the  source  of  light  toward  which 
they  are  swimming.  (2)  It  also  occurs  when  the  illumination  is  de- 
creased by  cutting  off  light  from  some  other  source  than  that  toward 
which  they  are  swimming.  Thus  the  organisms  on  the  stage  of  the 
microscope  may  be  lighted  from  below,  by  the  substage  mirror,  and  at 
the  same  time  may  receive  light  from  the  window  at  one  side  of  the 
preparation.  They  swim  toward  the  window,  since  the  light  from  that 
quarter  is  much  stronger  than  that  from  below.  If  now  the  light  from 
below  is  suddenly  decreased  by  closing  the  iris  diaphragm,  the  Euglenae 
react  as  usual  by  turning  strongly.  This  is  notwithstanding  the  fact 
that  the  proportion  of  light  coming  from  the  window,  to  which  they 
were  oriented,  is  now  greater  than  before,  so  that  it  might  be  supposed 
that  they  would  remain  more  strongly  oriented  than  ever.  For  the  rest, 
the  disturbed  orientation  is  soon  restored.  (3)  The  reaction  occurs 
when  the  decrease  in  illumination  is  due  to  the  movements  of  the 
Euglenae  ;  that  is,  when  the  swimming  organisms  come  to  the  edge  of 
a  lighted  region  where  they  would,  if  the  course  were  continued,  pass 
into  the  darkness.     As  a  result  of  the  reaction  they  return  into  the  light. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  5 1 

The  reaction  occurs  at  a  decrease  in  illumination  not  only  when  the 
organisms  are  oriented  and  swimming  toward  the  source  of  light,  but 
also  when  they  are  not  oriented  and  are  merely  scattered  in  a  weakly 
lighted  area.  Further,  in  cases  where  most  of  the  Euglenae  are  oriented 
and  swimming  toward  a  source  of  light,  a  number  of  specimens  will 
always  be  found  that  are  not  oriented  at  all,  or  are  swimming  away 
from  the  source  of  light.  Such  individuals  react  to  a  sudden  decrease 
in  illumination  in  the  same  manner  as  do  the  specimens  that  are  oriented 
with  the  anterior  end  toward  the  source  of  light.  This  result  may  be 
observed  in  a  curious  way  as  a  consequence  of  the  fact  that  it  requires 
some  time  for  the  light  to  produce  its  orienting  effect.  Thus,  if  the 
Euglenae  are  placed  between  a  weak  and  a  strong  light  they  swim  toward 
the  strong  light.  If,  now,  the  strong  light  is  cut  off,  they  react  in  the 
usual  way  and  swim  toward  the  weak  light.  Now  the  strong  light 
maybe  restored  ;  the  Euglenas  continue  for  a  few  seconds  to  swim  toward 
the  weak  light,  thus  away  from  the  strong  light.  If  while  they  are 
swimming  in  this  manner  the  strong  light  is  cutoff,  the  Euglenae,  swim- 
ming away  from  it,  react  in  the  usual  manner,  by  turning  strongly 
toward  the  dorsal  side. 

The  usual  reaction  may  be  produced  by  a  decrease  in  illumination 
that  is  not  sufficient  to  cause  a  permanent  change  in  orientation.  Thus 
the  Euglenae  on  a  slide  or  in  a  shallow  dish  may  be  lighted  from  a 
window  at  one  side.  By  passing  a  small  screen  in  front  of  the  window 
at  some  distance  from  the  preparation  a  portion  of  the  light  is  cut  off; 
the  Euglenae  then  respond  in  the  usual  way,  by  swerving  toward  the 
dorsal  side.  The  movement  thus  becomes  very  irregular.  Since  the 
Euglenae  continue  to  revolve  on  their  long  axes  the  dorsal  side  may  lie 
first  to  the  (observer's)  right,  then  to  the  left.  The  Euglenae  all  seem, 
therefore,  to  vibrate  from  side  to  side.  This  is  the  '' Erschiitterung  " 
or  trembling  described  by  Strasburger  (1878)  as  occurring  in  swarm- 
spores  when  the  illumination  is  changed  ;  it  will  be  understood  better 
when  we  have  considered  more  in  detail  the  mechanism  of  the  reactions. 
Meanwhile  the  screen  retains  its  position,  but  still  admits  more  light 
from  the  direction  of  the  window  than  from  any  other  direction.  The 
reaction  of  the  Euglenae,  therefore,  soon  ceases ;  their  orientation  is 
restored  in  the  way  to  be  described  later,  and  they  continue  to  swim 
toward  the  window. 

This  experiment  is  an  important  one.  It  shows  that  the  typical  reac- 
tion may  be  produced  by  a  decrease  in  light  that  is  not  sufficient  to 
permanently  destroy  the  orientation.  Thus  it  is  clearly  the  decrease 
in  illumination  to  which  the  organisms  react ;  not  to  a  change  in  the 
direction  of  the  light  rays.  The  experiment  shows  further  that  it  is 
not  the  absolute  amount  of  light  that  determines  the  reaction.     Some 


53  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

time  after  the  decrease  in  illumination  takes  place  the  organisms  behave 
just  as  they  did  before,  swimming  in  the  same  direction.  Further, 
the  illumination  may  be  decreased  very  slowly  to  the  same  extent 
without  causing  a  reaction.  If  the  screen  is  at  first  far  away  from  the 
preparation  and  is  then  slowly  moved  to  the  position  it  occupied  in 
the  experiment  just  described  no  reaction  is  produced.  It  is  only  the 
sudden  change  that  has  caused  the  reaction.  The  change,  however, 
need  not  be  a  very  marked  one  in  order  to  be  effective. 

Our  experiments  thus  far  have  shown  that  in  a  moderate  light  Eu- 
glena  reacts  to  a  decrease  in  illumination.  But  the  absolute  amount  of 
light  present  has  an  effect  on  the  reaction.  If  the  light  is  very  strongly 
increased  the  same  reaction  is  produced  as  when  the  light  is  decreased. 
If  while  the  organisms  are  swimming  toward  a  moderately  lighted 
window  direct  sunlight  is  allowed  to  fall  upon  them,  they  respond  in 
the  same  way  as  to  a  sudden  decrease  in  illumination  ;  that  is,  they 
turn  strongly  toward  the  dorsal  side,  continuing  or  repeating  the  re- 
action till  the  anterior  end  is  directed  away  from  the  source  of  light. 
They  now  continue  to  swim  in  that  direction,  the  positive  reaction 
having  been  transformed  into  a  negative  one.  Thus  under  intense 
light  the  conditions  of  stimulation  are  the  opposite  of  those  under 
moderate  light.  This  is  paralleled  in  the  reactions  of  the  infusoria  to 
chemicals  ;  often  a  strong  solution  of  a  certain  chemical  produces  a  re- 
action under  opposite  conditions  from  those  in  which  a  weak  solution 
of  the  same  chemical  is  effective. 

Let  us  now  proceed  to  a  more  careful  study  of  the  reaction  itself. 
The  reaction  which  occurs  when  the  illumination  is  changed  is  really 
an  accentuation  of  a  certain  feature  of  the  usual  movements.  Euglena, 
as  we  know,  revolves  on  its  long  axis  as  it  swims  forward,  and  at  the 
same  time  it  swerves  toward  the  dorsal  side.  The  resulting  path  is 
therefore  a  spiral  one  (Fig.  20).  The  usual  reaction  to  a  stimulus  is 
an  accentuation  of  this  normal  swerving  toward  the  dorsal  side,  as  com- 
pared with  the  other  factors  in  the  swimming;  the  organism  suddenly 
swerves  so  much  farther  than  usual  in  this  direction  that  the  path  may 
be  completely  changed.  If  the  reaction  is  a  very  decided  one  the  revo- 
lution on  the  long  axis  and  the  movement  forward  may  cease  during 
the  swerving  toward  the  dorsal  side ;  the  anterior  end  then  describes 
the  arc  of  a  circle  about  the  posterior  end  as  a  center.  In  a  less  pro- 
nounced reaction  the  revolution  on  the  long  axis  continues.  The  circle 
described  by  the  anterior  end  is  then  less  and  the  whole  body  describes 
the  surface  of  a  cone,  or  a  frustum  of  a  cone,  as  illustrated  in  Fig.  21. 
Every  gradation  exists  between  the  normal  spiral  course  and  the  strong 
reaction  in  which  the  anterior  end  swings  in  a  circle  about  the 
posterior  end  as  a  center. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


53 


When  oriented  and  swimming  toward  the  source  of  light  the  swerv- 
ing toward  the  dorsal  side  is  comparatively  slight.  As  seen  from 
above,  the  organisms  seem  merely  to  oscillate  a  very  little  from  side  to 
side  as  they  revolve  on  the  long  axis.  Careful  examination  shows  that 
the  swerving  is  always  toward  the  dorsal  side,  as  in  Fig.  20,  the  alter- 
nations in  direction  being  due  to  the  alternations  of  position  of  the 
dorsal  side.  Now,  when  the  illumination  is  suddenly  decreased,  the 
Euglenae  at  once  swing  much  farther  than  usual  toward  the  side  to 


Fig.  21.* 

which  they  are  already  swerving,  that  is,  toward  the  dorsal  side.  If 
the  decrease  in  illumination  is  not  very  great,  so  that  the  stimulus  is 
not  a  strong  one,  the  swerving  is  not  very  great,  and  the  organism  at 
the  same  time  continues  to  revolve  on  its  long  axis  ;  thus  the  anterior 
end  describes  a  circle  and  the  whole  body  describes  the  surface  of  a 


*FiG.  21. — Diagram  to  illustrate  reaction  of  Euglena  when  the  illumination 
is  decreased.  The  Euglena  is  swimming  forward  at  i ;  when  it  reaches  the 
position  2  the  illumination  is  decreased.  Thereupon  the  organism  swerves 
strongly  toward  the  dorsal  side.  This  swerving,  cotnbined  with  the  revolution 
on  the  long  axis,  causes  the  anterior  end  to  swing  about  a  circle,  so  that  the 
Euglena  occupies  successively  the  positions  2,  3,  4,  5.  6,  etc.  From  any  of  these 
positions  it  may  start  forward,  as  indicated  by  the  arrows,  if  the  condition 
causing  the  reaction  ceases  to  act.  In  the  figure  the  Euglena  is  represented  as 
swimming  forward  from  the  position  6. 


54 


THE    BKMAVIOR    OP    LOWER    ORGANISMS. 


cone,  or  the  frustum  of  a  cone,  as  indicated  in  Fig.  21.  The  result,  as 
seen  from  above,  is  that  all  the  specimens  seem  to  vibrate  from  side  to 
side  ;  in  other  words,  they  are  taken  with  a  sudden  oscillation  or  trem- 
bling. This  oscillation  when  the  intensity  of  the  light  is  suddenly 
changed  was  observed  by  Strasburger  (1878, 
pp.  25  and  50)  in  flagellate  swarm-spores ;  he 
speaks  of  it  as  "  Erschiitterung "  or  "  Zit- 
tern."  During  this  oscillation  the  anterior  end 
becomes  pointed  successively  in  many  different 
directions,  as  Fig.  21  shows.  When,  now,  the 
usual  forward  course  is  resumed  (with  only  the 
usual  amount  of  swerving  toward  the  dorsal 
side),  the  animal  follows  one  of  these  directions. 
Thus  its  path  is  changed  (Fig.  22).  Strasburger 
(187S,  p.  25)  noticed  that  the  path  followed  after 
the  oscillation  was  oblique  to  the  former  path. 
As  a  study  of  Figs.  21  and  22  will  show,  this  is  a 
necessary  consequence  of  the  increased  swerving 
toward  the  dorsal  side,  to  which  the  oscillation 
itself  is  due.  All  these  relations  become  much 
clearer  if  a  model  of  an  actual  spiral  is  studied  ; 
it  is  difficult  to  represent  them  upon  a  plane 
surface. 

If  the  stimulus  is  stronger,  as  when  there  is  a 
greater  decrease  in  illumination,  the  swerving 
toward  the  dorsal  side  is  much  greater ;  the  or- 
ganism wheels  far  to  that  side,  so  that  the  spiral 
course  seems  entirely  interrupted.  But  there  is 
really  nothing  in  this  reaction  differing  in  prin- 
ciple from  what  is  happening  in  the  normal 
forward  swimming.    If  the  swerving  toward  the 

f  dorsal  side  is  long  continued  the  specimen  may 

be  seen  to  swing  first  far  to  the  (observer's)  right, 

_  ^  then,  after  it  has  revolved  on  the  lone  axis,  far 

Fig.  22.*  '  fc>  ' 

to  the  (observer's)  left;  in  reality  it  swings  an 
equal  amount  upward  and  downward  and  in  intermediate  directions. 
It  may,  however,  swing  at  once  so  far  to  the  dorsal  side  that  the  new 


♦  Fig.  22. — Shows  the  spiral  path  of  Euglena,  illustrating  the  effect  of  a 
slightly  marked  reaction.  At  a  the  illumination  is  decreased;  the  organism 
therefore  swerves  toward  the  dorsal  side,  causing  the  spiral  to  become  wider. 
At  b  the  ordinary  method  of  swimming  is  resumed;  since  at  this  point  the 
organism  was  more  inclined  to  the  axis  of  the  spiral  than  before  the  reaction, 
the  new  course  lies  at  an  angle  with  the  previous  one.     Compare  with  Fig.  21. 


REACTIONS   TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


55 


course  forms  a  right  angle,  or  a  still  greater  angle,  with  the  original 
course;  if  the  turning  is  through  i8o°,  the  course  will  be  squarely 
reversed.  Indeed,  sometimes  the  organism  swings  around  an  entire 
circle  or  more.  When  the  usual  method  of  swimming  is  resumed  after 
such  reactions  as  those  just  described,  the  course  has  been  completely 
changed. 

Strasburger  (1S78,  p.  25)  noticed  that  after  a  decrease  in  illumina- 
tion flagellate  swarm-spores  often  turn  strongly  to  one  side  or  even 
describe  circles.  But  he  did  not  notice  that  the  turning  was  always 
toward  the  same  side  of  the  organism,*  and  did  not  perceive  the  relation 
between  this  effect  and  the  remainder  of  the  reaction. 


Fig.  23.1 

This  method  of  reaction  is  particularly  striking  when  the  Euglenae 
are  confined  to  a  very  thin  layer  of  water  between  the  slide  and  the 
cover  glass,  so  that  they  cannot  swerve  up  or  down.  When  the  light 
is  decreased,  we  will  suppose  that  the  dorsal  side  is  to  the  (observer's) 
left.     The  Euglena  then   swings  far  to  the  left.     At  the  same  time  it 


♦Naegeli  (i860,  p.  96)  had,  however,  before  Strasburger,  observed  that  in  such 
svi^arm-spores  the  same  side  always  faces  the  outside  of  the  spiral  path.  This 
observation,  which  really  contained  the  germ  of  a  correct  understanding  of  the 
reactions  to  stimuli,  seems  hardly  to  have  been  noticed  by  later  writers. 

t  Fig.  23. — Diagram  of  the  method  by  which  Euglena  becomes  oriented  with 
anterior  end  toward  the  source  of  light.  At  i  the  Euglena  is  swimming  toward 
the  source  of  light.  When  it  reaches  the  position  2  the  light  is  changed  so  as 
to  come  in  the  direction  indicated  by  the  arrows  at  the  right.  As  a  consequence 
of  the  decrease  in  illumination  of  the  anterior  end  thus  caused,  the  organism 


56  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

revolves  on  its  long  axis,  bringing  the  dorsal  side  down.  Since  it  can 
not  swing  downward,  owing  to  the  narrow  space,  this  has  little  effect 
on  the  reaction,  save  to  stop  the  movement  to  the  left.  Now,  by  con- 
tinued rotation  the  dorsal  side  has  come  to  lie  to  the  (observer's) 
right ;  the  Euglena  may  then  be  seen  to  swing  far  to  the  right.  In  each 
case  under  these  conditions  it  is  at  once  evident  by  observing  the 
larger  lip  at  the  anterior  end  that  the  organism  is  swinging  toward 
the  dorsal  side. 

This  method  of  reaction  is  very  effective  in  preventing  Euglena  from 
passing  from  an  illuminated  region  to  a  shaded  one.  As  soon  as  the 
anterior  end  enters  the  shadow,  the  animal  swings  far  toward  the  dor- 
sal side  till  the  anterior  end  is  brought  again  into  the  light,  repeating 
the  reaction  if  necessary.  There  is  then  no  further  cause  for  reaction. 
The  reaction  to  a  very  strong  increase  of  illumination  is,  as  we  have 
seen,  identical  with  that  to  a  decrease  in  illumination. 

In  our  experiments  thus  far  we  have  directed  attention  primarily  to 
the  effects  of  changes  in  the  intensity  of  illumination,  and  have  found 
that  such  changes  produce  a  motor  reaction  independently  of  the  direc- 
tion of  the  light  rays.  But  it  is  of  course  well  known  that  Euglena 
does  react  with  reference  to  the  direction  of  the  light  rays.  Euglenae 
swim  toward  the  source /^f  light  when  weakly  illuminated,  away  from 
the  source  of  light  when  strongly  illuminated.  If  Euglenae  are  swim- 
ming at  random  in  a  diffuse  light  they  soon  become  oriented  when  the 
light  is  allowed  to  act  on  them  from  one  side,  even  if  the  intensity  of 
illumination  remains  the  same.  Or,  if  Euglenae  are  swimming  toward 
a  source  of  very  weak  light  and  a  stronger  light  is  allowed  to  act  upon 
them  from  the  opposite  side,  they  become  oriented,  in  time,  with 
anterior  ends  toward  the  stronger  light.  In  examining  this  dependence 
of  the  direction  of  swimming  on  the  direction  of  the  rays  of  light,  we 


swerves  strongly  toward  the  dorsal  side,  at  the  same  time  continuing  to  revolve 
on  the  long  axis.  It  thus  occupies  successively  the  positions  2,  3,  4,  5,  6.  In 
passing  from  3  to  6  the  illumination  of  the  anterior  end  is  increased;  hence  the 
reaction  nearly  or  quite  ceases.  In  the  next  phase  of  the  spiral,  therefore,  the 
organism  swerves  but  a  little  toward  the  dorsal  side — from  7  to  8.  But  this 
movement  causes  a  decrease  in  the  illumination  of  the  anterior  end,  and  this 
change  induces  again  the  strong  swerving  toward  the  dorsal  side.  Hence  in 
the  next  phase  of  the  spiral  the  organism  swings  through  9  and  10  to  11.  In 
this  movement  again  the  illumination  of  the  anterior  end  is  increased;  hence 
the  reaction  ceases,  so  that  from  12  the  organism  swerves  only  as  far  as  13. 
Then  owing  to  the  decrease  in  illumination  caused  by  this  movement,  the 
swerving  increases,  so  that  the  Euglena  swings  from  13  through  14  and  15  to  16. 
Now  it  is  directed  toward  the  source  of  light,  and  such  swerving  as  takes  place 
in  the  spiral  course  neither  increases  nor  decreases  the  illumination  of  the 
anterior  end.  Hence  there  is  no  further  reaction;  the  Euglena  continues  to 
swim  forward  in  the  direction  16-17. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


57 


shall  have  to  keep  in  mind  two  questions :  First,  how  is  the  position 
of  orientation  brought  about?  Second,  what  is  the  real  stimulus  in 
producing  orientation  ? 

To  answer  the  first  question  we  must  observe  the  movements  of  the 


V-.?.-c^' 


M 


""^^^ 


<^^' 


'^^^ 


)a 


f—-4 


Fig.  24.* 

organism  at  the  time  orientation  occurs.  Observation  of  the  individ- 
uals as  they  are  becoming  oriented  shows  that  orientation  is  brought 
about  through  the  same  motor  reaction  that  we  have  already  described  ; 


*  Fig.  24. — Path  followed  by  Euglena  when  the  direction  of  the  light  is 
changed.  From  i  to  2  the  organism  swims  forward  in  the  usual  spiral  path. 
At  2  the  position  of  the  source  of  light  is  changed,  so  that  it  now  comes  from 
behind.     The  organism  then  begins  to  swerve  farther  than  usual  toward  the 


58  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

that  is,  by  a  turning  toward  the  dorsal  side.  The  simplest  case  is  per- 
haps that  of  the  reversal  of  orientation,  produced  when  strong  sunlight 
is  allowed  to  fall  from  in  front  upon  specimens  that  are  swimming 
toward  a  diffusely  lighted  window.  Under  these  circumstances,  as 
we  have  seen,  the  Euglenas  turn  toward  the  dorsal  side,  changing  their 
course.  They  may  turn  directly  through  180°,  in  which  case  they  are 
at  once  oriented  with  anterior  ends  away  from  the  light ;  but  usually 
the  orientation  is  less  direct  than  this.  The  reaction  is  generally 
repeated  several  times.  Through  its  continued  swerving  toward  the 
dorsal  side,  combined  with  the  revolution  on  the  long  axis,  the  organism 
directs  its  anterior  end  successively  in  every  direction.  When  the 
anterior  end  has  finally  come  into  a  position  where  it  points  away  from 
the  strong  light  the  reaction  ceases,  and  the  organism  swims  forward 
in  the  usual  way.  The  details  of  the  orienting  reaction  will  be  brought 
out  more  fully  in  the  following  account  of  the  way  in  which  the  anterior 
end  becomes  directed  toward  a  source  of  light  of  moderate  intensity. 
Let  us  now  take  a  case  in  which  the  change  in  the  direction  of  the 
rays  of  light  is  not  accompanied  by  a  change  in  the  intensity  of  illumi- 
nation. Euglense  are  swimming  about  at  random  in  a  diffuse  light 
when  all  the  light  is  allowed  to  fall  upon  them  from  one  side.  They 
then  become  oriented,  with  anterior  ends  directed  toward  the  source  of 
light  Or,  the  organisms  are  swimming  toward  a  source  of  light  when 
the  direction  of  the  light  rays  is  changed  or  reversed  by  quickly 
moving  the  source  from  which  the  light  comes.  The  Euglenae  then 
after  a  time  become  reoriented.  Under  such  circumstances  there  is  no 
sudden,  decided  reaction,  such  as  occurs  when  the  illumination  is 
suddenly  decreased.  The  organism  merely  begins  to  swerve  farther 
toward  the  dorsal  side  than  usual.  Thus  the  spiral  has  become  wider, 
and  the  anterior  end  comes  to  be  pointed  successively  in  many  dif- 
ferent directions,  as  illustrated  at  1-6  in  Fig.  23.  In  some  of  these 
positions  the  anterior  end  is  directed  farther  away  from  the  source 
of  light,  as  at  3  ;  in  other  positions  more  nearly  toward  the  source 
of  light,  as  at  6.  In  the  latter  case  the  swinging  toward  the  dorsal 
side  becomes  less  marked  ;  hence  the  succeeding  phase  of  the  swing, 
which  carries  the  anterior  end  away  from  the  light,  is  less  pronounced  ; 


dorsal  side,  owing  to  the  decrease  in  the  illumination  of  the  anterior  end.  Thus 
the  spiral  becomes  wider,  a  and  b  showing  the  limits  of  the  swerving.  At  3  the 
normal  amount  of  swerving  is  restored,  so  that  the  new  path  is  at  an  angle  with 
the  old  one.  Now  the  organism  swerves  at  each  turn  of  the  spiral  a  short  dis- 
tance away  from  the  source  of  light,  as  at  c,  e,  g,  and  a  longer  distance  toward 
the  source  of  light,  as  at  d,f,  h^  for  the  reasons  shown  in  Fig.  23.  At  h  it  has 
in  this  manner  become  directed  toward  the  source  of  light,  and  there  is  no  fur- 
ther cause  for  swerving  more  to  one  side  than  to  the  other;  it  therefore  swims 
in  a  spiral  with  a  straight  axis  toward  the  source  of  light. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  59 

the  anterior  end  therefore  does  not  swing  so  far  in  the  direction 
away  from  the  light  as  in  the  preceding  phase  it  swung  toward  the 
light.  This  is  illustrated  at  7-8  in  Fig.  23.  But  as  a  result  of  such 
swerving  as  does  occur  the  anterior  end  is  now  (at  8)  directed  more 
away  from  the  source  of  light  than  before.  There  then  follows  a 
new  reaction,  with  increased  swerving  toward  the  dorsal  side  in  the 
next  phase  of  the  spiral  (8-1 1,  Fig.  23),  which  carries  the  dorsal  side 
toward  the  source  of  light.  Hence  the  anterior  end  swings  still  further 
toward  the  position  where  the  light  shines  directly  upon  it.  This  con- 
tinues. As  a  result  of  this  repeated  swinging  of  the  dorsal  side  slightly 
away  from  the  source  of  light  and  strongly  toward  the  source  of  light 
the  organism  gradually  changes  its  course,  continuing  to  swim  in  a 
spiral  and  to  swerve  toward  the  dorsal  side,  until  the  axis  of  the  spiral 
is  in  line  with  the  light  rays  and  the  anterior  end  is  toward  the  source 
of  light.  This  method  of  reaction  will  best  be  understood  by  a  study 
of  Figs.  23  and  24  and  their  explanation. 

Thus  the  orientation  is  gradual  and  for  a  certain  stretch  after  the 
light  has  begun  to  act  the  organism  is  not  completely  oriented.  With 
a  fairly  strong  light,  however,  the  period  of  time  required  for  complete 
orientation  is  very  slight.  Strasburger  (1878,  p.  24)  noticed  that  when 
Haematococcus  is  swimming  toward  a  source  of  weak  light  and  the 
light  is  suddenly  increased  so  as  to  reverse  the  orientation,  there  is  a 
period  of  "  verschiedenen  Schwankungen  "  before  the  reverse  orienta- 
tion is  attained.  He  paid  little  attention  to  the  behavior  of  the 
organisms  during  this  period,  however. 

Our  account  has  been  thus  far  purely  descriptive  ;  we  have  attempted 
to  set  forth  the  events  as  they  may  be  observed ,  without  trying  to 
indicate  the  causes  at  work.  We  must  now  inquire  as  to  what  is  the 
real  stimulus  and  its  method  of  action  in  producing  orientation. 

First,  we  note  that  in  becoming  oriented  Euglena  does  not  turn 
directly  toward  the  source  of  light.  As  in  the  reaction  to  other  stimuli, 
the  turning  is  throughout  toward  a  structurally  defined  side.  This 
shows  that  the  orientation  of  Euglena,  like  that  of  Stentor,  cannot  be 
accounted  for  on  the  orthodox  tropism  theory.  In  other  words,  the 
orientation  is  not  due  to  the  direct  effect  of  the  light  on  the  motor 
organs  of  the  side  on  which  it  falls.  As  in  Stentor,  orientation  may 
be  reached  by  turning  either  toward  or  away  from  the  source  of  light, 
or  in  any  intermediate  direction.  The  response  is  a  "  motor  reaction  '* 
of  a  definite  type. 

Just  what  is  the  stimulus  which  produces  this  motor  reaction.?  All 
our  experiments  up  to  this  point  have  shown  clearly  that  this  reaction 
is  produced  by  changes  in  the  intensity  of  illumination,  and  that  a  change 
in  the  illumination  of  the  anterior  end  produces  the  reaction  as  well  as 


6o  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

does  a  change  in  the  illumination  of  the  entire  body.  Indeed,  Engel- 
mann  (18S2,  a)  showed  that  a  change  in  illumination  over  the  remainder 
of  the  body  is  ineffective  in  producing  the  reaction,  so  that  in  every  case 
the  reaction  is  due  to  the  change  in  illumination  at  the  anterior  end. 
Now,  in  the  orientation  reaction  the  conditions  are  present  for  produc- 
ing changes  of  illumination  at  the  anterior  end  of  precisely  the  character 
which  would,  in  view  of  our  other  experimental  results,  bring  about 
the  reactions  observed.  This  will  best  be  shown  by  again  examining 
in  detail  from  this  point  of  view  a  concrete  case. 

In  Fig.  23  we  will  suppose  that  the  Euglena  at  i  is  at  first  swimming 
toward  the  source  of  light.  When  it  reaches  the  position  2  the  light  is 
changed,  so  that  it  now  comes  from  the  direction  indicated  by  the 
arrows  at  the  right.  By  this  change  the  intensity  of  illumination  at 
the  anterior  end  is  decreased,  since  before  the  light  came  from  directly 
in  front  and  affected  the  entire  end,  while  now  it  falls  upon  but  one 
side.  We  know  from  other  experiments  that  as  a  result  of  such  a 
change  the  organism  reacts  by  swerving  more  toward  the  dorsal  side, 
at  the  same  time  continuing  to  revolve  on  the  long  axis.  This  is  ex- 
actly what  happens  now  ;  by  the  increased  swerving  the  organism  is 
carried  from  position  2  to  position  3.  In  this  change  the  anterior  end, 
swinging  still  farther  away  from  the  source  of  light,  is  still  less  illumi- 
nated than  before.  As  a  result  of  this  farther  decrease  in  illumination 
the  reaction  is  continued  or  increased ;  combined  with  the  revolution 
on  the  long  axis  it  carries  the  organism  successively  to  positions  4,  5 
and  6.  In  this  part  of  the  movement  the  anterior  end  becomes  pointed 
more  directly  toward  the  source  of  light,  and  is  hence  more  strongly 
illuminated ;  there  is  therefore  nothing  in  this  movement  to  cause  a 
reaction.  The  strong  swerving  toward  the  dorsal  side  then  ceases  or 
becomes  less.  But  in  the  next  phase  of  the  spiral  course  (from  7  to  8), 
there  is  necessarily  at  least  the  normal  amount  of  swerving  toward  the 
dorsal  side,  and  this  carries  the  organism  to  a  position  (8),  where 
the  intensity  of  the  light  acting  on  the  anterior  end  is  decreased.  As 
a  result  of  this  decrease  we  know  that  the  "  motor  reaction  "  must  again 
be  induced ;  the  organism  swings  then  farther  toward  the  dorsal  side* 
This  movement,  combined  with  the  revolution  on  the  long  axis,  carries 
the  Euglena  through  9  and  10  to  11.  Here  again  the  swerving  de- 
creases, because  the  change  was  from  a  less  illuminated  to  a  more 
illuminated  region.  Hence  after  reaching  12  the  Euglena  swerves  only 
a  little  away  from  the  light,  to  13  ;  then,  as  a  result  of  the  decrease  in 
illumination  at  the  anterior  end  caused  by  this  movement,  it  swerves 
far  toward  the  light,  through  14  and  15  to  16.  This  movement  causing 
greater  illumination,  the  reaction  ceases.  The  light  is  now  shining  full 
on  the  anterior  end.     The  organism  therefore  swims  forward  in  the 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  6l 

usual  spiral  course,  in  all  phases  of  which  the  illumination  of  the  anterior 
end  is  equal.  If  the  light  came  from  the  rear  of  Euglena  i  instead  of 
from  the  direction  indicated  by  the  arrows,  the  reaction  above  described 
would  be  continued  in  the  same  way  until  the  direction  of  swimming 
was  completely  reversed. 

Thus  the  orientation  of  Euglena  in  a  continuous  light  is  due  to  the 
production  of  the  *'  motor  reaction,"  with  its  turning  toward  the  dorsal 
side,  whenever  there  is  a  decrease  in  illumination  at  the  anterior  end. 

There  is  no  other  explanation  of  the  orientation,  so  far  as  I  am  able 
to  see,  that  is  in  agreement  with  all  the  facts.  At  first  one  is  tempted 
merely  to  say  that  the  subjection  of  the  anterior  end  to  shadow  pro- 
duces the  motor  reaction,  and  that  this  is  continued  until  the  anterior 
end  is  no  longer  shaded.  This  statement  is  correct  if  by  "subjection 
to  shadow*'  we  mean  an  active  process,  involving  a  change  from  a 
more  illuminated  condition.  But  if  we  mean  that  darkness  as  a  con- 
tinuous, static  condition  is  the  cause  of  the  reaction,  then  considera- 
tion shQws  that  this  will  not  account  for  all  the  facts.  It  leaves  out  of 
account  the  capability  of  the  organism  to  become  acclimatized  to  cer- 
tain degrees  of  light  and  shade,  and  certain  of  the  experimental  results 
are  crucial  against  it.  Thus,  suppose  the  Euglenas  are  swimming 
toward  a  source  of  weak  light,  and  a  stronger  light  is  then  allowed  to 
act  upon  them  from  another  direction.  The  anterior  end  continues  to 
receive  the  same  amount  of  light  as  before  (since  the  weak  light  still 
persists),  yet  the  organism  reacts  as  usual,  becoming  oriented  toward 
the  stronger  light.  The  motor  reaction  by  which  the  orientation  is 
brought  about  cannot  therefore  be  due  to  darkness  or  shade  (considered 
statically)  at  the  anterior  end.  On  the  other  hand,  the  case  just  men- 
tioned is  easily  understood  on  applying  the  explanation  given  above. 

Again,  it  might  be  held  that  the  reaction  is  due  in  some  way  to  the 
relative  amount  of  illumination  at  the  two  ends.  It  might  be  main- 
tained, for  example,  that  when  the  posterior  end  is  more  illuminated 
than  the  anterior,  this  difference  acts  as  a  stimulus  to  cause  the  '*  motor 
reaction."  There  is,  of  course,  no  independent  evidence  in  favor  of  this 
view,  and  the  experimental  results  prove  it  to  be  incorrect.  We  have 
shown  that  the  reaction  is  produced  (i)  when  both  ends  are  equally 
stimulated,  as  when  the  light  comes  directly  from  one  side  ;  (2)  when 
neither  end  receives  light,  as  when  the  light  is  cut  off  completely.  Fur- 
ther, it  might  be  held  that  the  reaction  is  produced  when  the  anterior  end 
is  not  more  intensely  illuminated  than  the  posterior  end.  It  is,  of  course, 
a  little  difficult  to  conceive  how  so  indefinite  a  condition  could  act  as  a 
stimulus  to  a  definite  motor  reaction,  but  in  any  case  the  experiments  show 
that  this  is  not  the  real  cause  of  the  ''  motor  reaction."  Thus  certain  of 
the  experiments  show  that  the  "  motor  reaction  "  is  produced  even  when 


63  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  light  is  reduced  by  the  same  amount  at  both  ends,  so  that  the  anterior 
end  is  still  more  strongly  lighted  than  the  posterior.  This  case  is 
realized  in  the  experiment  in  which  a  small  screen  is  interposed  between 
the  EuglenaB  and  the  window  toward  which  they  are  swimming.  The 
light  is  thus  somewhat  decreased,  but  is  still  sufficient  to  cause  orien- 
tation. The  anterior  end  is  thus  still  lighted  more  than  the  posterior, 
yet  the  organisms  respond  with  the  "  motor  reaction"  at  the  moment 
the  light  is  decreased.  The  same  thing  is  shown  still  more  decidedly 
in  the  experiment  described  on  page  50,  in  which  the  "  motor  reaction  " 
is  produced  when  the  light  is  cut  off  from  some  other  source  than  that 
toward  which  the  organisms  are  swimming.  In  this  case  the  propor- 
tion of  light  shining  on  the  anterior  end  is  greater  after  the  change  in 
illumination  than  before,  yet  the  *'  motor  reaction"  is  produced  at  the 
moment  the  change  takes  place. 

The  explanation  we  have  given  is,  therefore,  the  only  one  that  is  in 
agreement  with  all  the  facts,  and  it  accounts  for  every  detail  of  the  re- 
actions to  light.  The  cause  of  all  the  phenomena  of  light  reaction  in 
Euglena  is  the  fact  that  a  sudden  change  in  light  intensity  on  the  anterior 
end  induces  a  typical  ''  motor  reaction."  It  is  noticeable  that  the 
reaction  is  throughout  due  to  a  dynamic  factor,  to  some  change  in  the 
relation  of  the  organism  to  the  light,  a  change  due  either  to  an  active 
alteration  of  the  environment,  or  to  a  movement  of  the  organism.  To 
static  conditions,  if  not  too  intense,  the  organism  may  soon  become 
acclimatized,  so  that  no  farther  reaction  is  caused.  The  absolute  in- 
tensity of  the  light  affects  the  reaction  only  in  so  far  as  it  determines 
whether  it  shall  be  an  increase  or  a  decrease  in  intensity  that  causes 
the  *'  motor  reaction." 

To  sum  up,  the  reaction  of  Euglena,  from  beginning  to  end,  is  ex- 
plained by  the  fact  that  a  sudden  change  in  illumination,  even  though 
slight,  causes  a  definite  motor  reaction,  the  essential  feature  of  which 
is  an  increased  swerving  toward  the  dorsal  side.  Orientation  is  brought 
about  by  the  increased  swerving  in  the  next  phase  of  the  spiral  course 
when  the  illumination  of  the  anterior  end  is  diminished,  and  by  the 
decreased  swerving  in  the  next  phase  of  the  spiral  when  the  illumination 
of  the  anterior  end  is  increased.  In  general  terms  we  can  say  that  the 
reaction  of  Euglena  to  light  is  by  the  method  of  trial  and  error.  The 
organism  tries  turning  in  many  directions ;  when  the  turning  is  such 
as  to  produce  a  decrease  in  the  illumination  of  the  anterior  end  it 
**  tries"  other  directions;  when  it  is  such  as  to  produce  increased 
illumination  of  the  anterior  end,  or  when  no  change  in  illumination 
results,  the  reaction  ceases  and  the  organism  continues  to  swim  forward 
in  that  position.  The  result  of  this  method  of  reaction  is  necessarily 
orientation  with  the  anterior  end  toward  the  source  of  light. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  63 

CRYPTOMONAS  AND  CHLAMYDOMONAS. 

Cryptomonas  ovata  is  one  of  the  organisms  studied  by  Strasburger 
(187S),  under  the  name  Chilomonas  ovata^  in  his  classical  paper  on 
reactions  to  light  in  flagellates  and  swarm-spores. 

The  specimens  studied  by  the  present  author  were  mostly  of  the 
*' young"  form,  having  pointed,  curved,  posterior  ends.  One  side  is 
strongly  convex,  while  the  other  is  less  curved,  or  is  even  concave  near 
the  posterior  end.  It  is  thus  very  easy  to  distinguish  the  two  sides  of 
the  organism  and  to  observe  their  relation  to  the  movements. 

Cryptomonas  ovata  swims  in  a  rather  wide  spiral,  with  the  more 
convex  side  toward  the  outer  surface  of  the  spiral.  In  other  words,  the 
organism  swerves  continually  toward  the  more  convex  side.  The 
response  to  usual  stimuli  is  a  strong  turn  toward  this  convex  surface ; 
this  is  easily  seen  when  the  organism  comes  in  contact  with  an 
obstacle. 

The  Cryptomonads  swim  toward  or  away  from  the  source  of  light 
under  the  same  conditions  as  Euglena,  and  gather  in  lighted  areas  in 
the  same  manner  as  does  the  organism  last  named.  They  react  to  a 
sudden  decrease  in  the  intensity  of  illumination  by  turning  toward  the 
more  convex  side.  If  the  decrease  in  intensity  is  marked,  the  organism 
turns  suddenly  for  a  long  distance,  90°  or  more,  so  that  the  course  is 
completely  changed.  If  the  stimulus  is  less  the  turning  toward  the 
more  convex  side  is  not  so  rapid,  and  since  the  revolution  on  the  long 
axis  is  continued  the  body  of  the  organism  describes  the  surface  of  a 
wide  cone  or  frustum  of  a  cone.  When  a  large  number  of  specimens 
react  in  this  way  at  the  same  time  a  peculiar  shaking  or  trembling 
appearance  is  produced;  this  is  evidently  what  Strasburger  (1878) 
called  "  Erschiitterung  "  or  "  Zittern."  As  a  consequence  of  the  wide 
swerving,  when  the  normal  method  of  swimming  is  resumed  the  course 
lies  in  a  new  direction. 

In  all  these  respects  Cryptomonas  exactly  resembles  Euglena.  Fur- 
ther, the  organism  becomes  oriented  to  light  in  precisely  the  same  manner 
as  is  described  above  for  Euglena.  In  fact,  if  we  substitute  "  more 
convex  side"  for  "  dorsal  side  "  in  the  account  of  Euglena,  it  will  fit 
almost  throughout  the  reactions  of  Cryptomonas.  It  is  therefore  unnec- 
essary to  describe  the  phenomena  in  Cryptomonas  in  detail. 

A  study  was  made  also  of  the  reactions  of  a  species  of  Chlamydo- 
monas.  The  movements  of  Chlamydomonas  and  its  reactions  to  light 
resemble  those  of  Euglena  and  Cryptomonas.  But  the  organism  is  so 
small  and  the  differentiations  of  the  bodily  structure  are  so  slight  that 
I  was  unable  to  determine  the  relation  of  its  structure  to  the  spiral 
path  and  to  the  direction  of  turning  in  the  reaction.     The  oriented 


©4  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

organism  reacts  to  a  decrease  in  illumination  by  a  sudden  turn  to  one 
side,  by  an  increase  in  the  width  of  the  spiral,  and  by  a  change  in  the 
course,  just  as  happens  in  Euglena  and  Cryptomonas.  The  unoriented 
organism  becomes  oriented  in  a  manner  which  is  similar  to  that  de- 
scribed above  for  the  two  organisms  just  named.  Since,  however,  I 
am  unable  to  give  the  precise  relations  of  these  movements  to  struc- 
tural differentiations  of  the  body,  a  further  account  of  details  would 
not  be  of  interest. 

GENERAL  RESULTS. 

In  summing  up  our  results  on  reactions  to  light  in  the  organisms 
studied,  there  are  two  points  of  especial  interest  which  should  be  con- 
sidered separately.  The  first  relates  to  the  nature  of  the  reaction 
produced,  the  second  to  the  nature  of  the  agent  causing  the  reaction. 

NATURE  OF  REACTION  PRODUCED  BY  LIGHT. 

As  to  the  nature  of  the  reaction  produced  by  light  there  has  been 
much  discussion.  The  orthodox  tropism  theory  is  perhaps  that  which 
has  the  greatest  number  of  adherents.  It  is  set  forth  in  detail  in  the 
paper  of  Holt  &  Lee  (1901).  According  to  this  theory  the  light  acts 
directly  on  the  motor  organs  of  the  side  on  which  it  impinges  ;  supra- 
optimal  light  causes  increase  of  the  backward  stroke  (in  the  case  of 
cilia  or  other  swimming  organs)  ;  suboptimal  light  causes  a  decrease 
in  the  backward  stroke.  The  result  is  that  the  organism  is  turned 
directly  toward  or  from  the  more  intensely  lighted  side,  and  hence 
toward  or  from  the  source  of  light.  The  diagrams  given  in  the  pre- 
ceding paper  (Figs,  i  and  2)  can  be  applied  directly  to  the  elucidation 
of  this  theory. 

In  the  experiments  on  the  ciliates  and  flagellates  set  forth  in  the 
present  paper  the  precise  method  of  reaction  was  determined  by  obser- 
vation. It  is  not  in  accordance  with  the  tropism  theory  above  set 
forth.  This  has  been  emphasized  in  detail  in  the  account  of  the 
reactions  of  Stentor,  so  that  it  need  not  be  reiterated  here.  The  reac- 
tion to  light  is  of  the  same  character  as  that  to  other  stimuli,  and  takes  the 
form  of  a  motor  reaction  in  which  the  organism  performs  a  definite 
set  of  actions.  It  first  usually  stops  or  swims  backward,  then  turns 
toward  a  structurally  defined  side,  then  continues  forward.  The 
result  is  to  change  the  course  of  the  organism.  As  a  result  of  the  con- 
tinual rotation  on  the  long  axis,  together  with  the  swerving  toward  a 
certain  side,  the  organism  comes  to  be  pointed  successively  in  every 
direction.  In  continues  to  swim  forward  in  that  direction  which  does 
not  induce  a  stimulus  to  further  swerving.  The  whole  reaction  is  a 
strongly  marked  example  of  the  type  of  behavior  which  may  be  called 
the  "  method  of  trial  and  error." 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  65 

NATURE  OF  AGENT  CAUSING  THE  REACTION. 

(i)  The  primary  and  essential  cause  of  the  reaction  is  a  change  of 
illumination.  The  change  of  illumination  must  take  place  with  some 
suddenness,  but  need  not  be  very  great  in  amount.  The  change  in 
illumination  acts  as  an  effective  stimulus  even  though  the  degree  of 
illumination  preceding  the  change  and  that  following  it  would,  when 
acting  continuously,  produce  no  such  result.  This  is  shown  by  the 
experiments  on  Euglena,  in  which  the  light  coming  from  one  side  was 
decreased  a  certain  amount.  The  orientation  of  the  organisms  and 
their  direction  of  movement  vvas  the  same  before  and  after  the  change, 
but  at  the  moment  the  change  occurred  there  was  a  marked  reaction. 
Other  experiments  detailed  above  demonstrate  the  same  thing.  Further, 
the  change  in  illumination  acts  independently  of  the  direction  of  the 
rays  of  light.  This  is  shown  by  the  experiment  just  cited,  in  which 
the  effective  direction  of  the  rays  of  light  was  the  same  before  and 
after  the  reaction  ;  it  is  also  shown  in  the  reaction  caused  when  the 
light  is  decreased  from  below,  in  the  case  of  Euglenae  swimming 
toward  a  window  (p.  50),  and  in  the  reaction  of  Stentor  on  passing  from 
a  shadow  to  a  lighted  region  even  when  the  animal  is  oriented  with 
anterior  end  away  from  the  light  (p.  39).  The  change  in  illumination 
acts  equally  whether  it  affects  the  entire  organism  or  only  the  anterior 
end.  The  evidence  indicates  that  in  all  cases  it  is  really  the  change  at 
the  anterior  end  which  induces  the  reaction. 

(2)  The  absolute  intensity  of  the  light  affects  the  reaction  by  deter- 
mining in  a  given  case  whether  a  reaction  shall  be  caused  by  an 
increase  or  a  decrease  in  illumination.  Through  this  action  it  also 
determines,  in  the  way  to  be  mentioned  in  the  next  paragraph,  whether 
in  a  continuous  light  the  sensitive  anterior  end  shall  be  directed  toward 
or  away  from  the  source  of  light ;  that  is,  whether  the  response  shall 
be  *' positive"  or  "negative." 

(3)  Indirectly,  and  through  the  factor  set  forth  in  paragraph  (i),  the 
direction  from  which  the  light  comes  is  a  determining  factor  in  the 
reactions.  Through  the  spiral  course  in  which  the  organisms  swim  such 
conditions  are  furnished  that  in  a  field  continuously  lighted  from  one 
side  the  sensitive  anterior  end  of  the  unoriented  organism  is  subjected 
to  repeated  changes  in  the  intensity  of  illumination.  As  a  result, 
organisms  which  respond  by  the  motor  reaction  to  an  increase  in  illu- 
mination at  the  anterior  end  must  become  oriented  with  anterior  end 
directed  away  from  the  light ;  organisms  which  react  to  a  decrease  in 
illumination  must  become  oriented  with  anterior  end  directed  toward 
the  light.  (Details  in  the  account  of  Euglena,  pp.  60,  61,  and  Figs. 
23,  24.) 


66  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

The  results  of  this  method  of  reacting  may  be  stated  correctly,  though 
not  completely,  as  follows :  In  a  negative  organism  light  falling  upon 
the  sensitive  anterior  end  causes  a  reaction  by  which  the  anterior  end 
is  pointed  in  many  different  directions ;  the  reaction  ceases  as  soon  as 
a  direction  is  reached  in  which  the  anterior  end  is  pointed  away  from 
the  light.  In  a  positive  organism  the  shading  of  the  sensitive  anterior 
end  produces  the  reaction  by  which  the  anterior  end  is  pointed  in  many 
different  directions ;  the  reaction  ceases  as  soon  as  the  anterior  end  is 
no  longer  shaded.*  The  reaction  is  thus  by  the  method  of  trial  and 
error ;  when  stimulated  the  organism  tries  many  different  positions, 
till  one  is  found  in  which  there  is  no  further  stimulation. 

Consideration  will  show,  I  think,  that  the  factors  producing  reaction 
to  light  in  these  lowest  organisms  are  essentially  the  same  as  in  higher 
ones,  if  man  may  be  taken  as  a  type  of  the  latter.  The  factors  are,  as 
we  have  seen,  variations  in  intensity  of  illumination,  and,  indirectly, 
the  direction  from  which  the  light  comes.  It  is  possible  that  in  man 
the  latter  factor  works  more  directly  than  in  the  infusoria  ;  leaving  this 
question  out  of  consideration,  the  two  factors  are  present  in  both  cases. 
Consider  a  human  being  who  reacts  to  light  as  a  purely  physical  agent, 
not  with  regard  to  the  associations  which  it  brings  up.  In  a  dark  space 
a  gleam  of  light  is  pleasant  and  induces  movement  toward  it.  There 
is  then  a  positive  reaction  with  orientation,  but  the  orientation  is  not 
due  to  the  difference  in  intensity  of  light  on  different  parts  of  the  body, 
nor  to  its  direct  effect  on  the  motor  organs.  The  orientation  is  such  as 
to  keep  the  light  shining  on  the  more  sensitive  part  of  the  body,  the 
eyes.  An  excessively  powerful  light  is  unpleasant  and  induces  a  nega- 
tive reaction  just  as  happens  in  Euglena ;  the  orientation  is  then  such 
as  to  keep  the  more  sensitive  part  of  the  body,  the  eyes,  away  from  the 
light.  Further,  man  is  sensitive  to  a  sudden  change  in  illumination. 
A  strong  light  bursting  from  the  darkness,  or  sudden  darkness  in  the 
midst  of  bright  light,  induces  a  marked  motor  reaction,  and  less  striking 
differences  may  produce  a  response.  Both  in  man  and  in  Euglena  the 
reaction  likewise  depends  upon  color  ;  but  with  this  phase  of  the  matter 
we  are  not  at  present  concerned. 

When  the  factors  above  set  forth  are  taken  into  consideration  certain 
peculiar  experimental  results  that  have  given  rise  to  much  discussion 
become  clearly  intelligible.  I  refer  particularly  to  the  experiments  in 
which  the  direction  of  the  light  and  the  decrease  in  intensity  of  illumi- 
nation do  not  show  the  usual  relations.  Under  ordinary  conditions 
movement  away  from  a  source  of  light  is  movement  into  a  region  of  less 

*  This  statement  is  incomplete  in  that  it  does  not  bring  out  the  fact  that  it  is 
a  change  from  light  to  shade  or  vice  versa  that  induces  the  reaction;  if  this  be 
understood,  the  statement  is  correct. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  6"] 

intensity  ;  movement  toward  the  light  into  a  region  of  greater  intensity. 
In  the  well-known  experiments  of  Strasburger  (1878)  and  others,  this 
condition  is  modified  by  passing  the  light  through  a  wedge-shaped 
prism  filled  with  a  solution  that  cuts  out  part  of  the  light. 

When  a  drop  of  water  or  a  culture  dish  is  placed  beneath  such  a 
prism,  and  the  latter  is  so  situated  that  its  surface  is  perpendicular  to 
the  light  rays,  the  intensity  of  the  illumination  is  greatest  behind  the 
thin  edge  of  the  prism,  and  thence  decreases  gradually  toward  the 
opposite  end,  while  the  rays  of  light  all  come  directly  from  above. 
Under  these  conditions  Strasburger  (1878,  p.  36)  found  that  the  positive 
swarm-spores  remained  equally  distributed  throughout  the  drop,  not 
collecting  at  the  lighter  end.  Now,  the  only  difference  between  this 
experiment  and  the  one  illustrated  in  Fig.  1 1  of  the  present  paper  is 
that  in  Strasburger*s  experiment  the  decrease  in  illumination  is  very 
gradual.  We  have  seen  above  (p.  52)  that  a  very  gradual  change  in 
illumination  produces  no  reaction.  Hence  the  organisms  may  wander 
from  one  side  of  the  drop  to  the  other  without  reaction,  the  difference 
in  illumination  at  two  successive  instants  never  rising  to  the  necessary 
threshold  of  stimulation.  If  the  relation  of  stimulus  to  reaction  follows 
Weber's  law,  the  result  is  just  what  we  should  expect,  provided  the 
change  in  illumination  is  sufficiently  gradual.  When  the  difference  in 
illumination  from  above  is  great,  Strasburger's  own  experiments  (/.  c, 
p.  33)  show  that  the  organisms  do  react. 

On  the  other  hand.  Holt  &  Lee  (1901),  using  a  similar  prism, 
found,  under  similar  conditions,  that  the  negative  organism,  Stentor, 
does,  on  the  whole,  tend  to  gather  at  the  darker  side  of  the  drop. 
This  shows  that  the  difference  in  illumination  between  neighboring 
points  in  this  particular  experiment  was  not  below  the  threshold  of 
stimulation  for  the  organism  in  question.  If,  as  Holt  &  Lee  sup- 
pose, a  certain  amount  of  light  was  reflected  from  the  lighter  end  of 
the  vessel,  then  the  inclination  to  go  to  the  darker  side  would  be  rein- 
forced by  Stentor's  tendency  to  turn  when  the  light  falls  upon  its 
anterior  end  (see  p.  43).  The  fact  that  in  Strasburger's  experiments 
the  organisms  remained  scattered  throughout  the  drop  seems  to  indi- 
cate that  this  reflected  light  played  no  part  in  his  results. 

In  another  set  of  experiments  Strasburger  placed  his  prism  over  the 
swarm-spores  in  such  a  way  that  the  light  came  obliquely  from  the 
direction  of  the  thick  end  of  the  wedge.  If  the  positive  organisms  now 
go  toward  the  thicker  end  of  the  wedge,  they  pass  toward  the  source 
of  light,  but  into  a  region  of  decreased  illumination  ;  if  they  go  toward 
the  thin  end  they  pass  away  from  the  source  of  light,  but  into  a  region 
of  higher  illumination.     Which  will  they  choose.? 

Strasburger  found  that  the  positive  swarm-spores  pass  toward  the 


68  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

source  of  light,  into  the  region  of  less  illumination.  But  is  not  this 
exactly  what  we  must  expect?  His  former  experiment  showed  us  that 
under  the  prism  the  change  from  light  to  darkness  was  so  gradual  that  it 
produced  no  effect  on  the  organisms.  Hence  the  direction  from  which 
the  rays  come  is  left  to  produce  its  effect  alone,  and  it  produces  the 
usual  effect.  The  organism  reacts  in  the  usual  "  trial  and  error"  way 
until  the  anterior  end  is  directed  toward  the  light ;  then  it  moves  in  that 
direction.  Incidentally  it  comes  into  a  region  of  less  intensity  of  light, 
though  the  decrease  is  so  slight  as  to  produce  no  effect  on  the  organism. 

Parallel  considerations  hold  for  the  negative  organism.  Under 
similar  circumstances,  if  the  variation  in  illumination  is  very  gradual, 
it  directs  its  sensitive  anterior  end  away  from  the  source  of  light  (by  the 
method  of  '*  trial  and  error")  and  swims  to  the  opposite  side  of  the 
drop,  incidentally  moving  into  a  region  of  slightly  greater  (but 
"  unperceived  ")  intensity  of  illumination.  Under  similar  conditions, 
as  we  have  seen  in  the  experiment  described  on  p.  39,  if  the  decrease 
in  illumination  is  marked,  the  animal  swims  back  into  the  shadow, 
though  in  so  doing  it  passes  toward  the  source  of  light. 

Thus  in  Strasburger's  experiments  with  the  prism  the  difference  in 
the  intensity  of  light  between  neighboring  regions  has  been  made  so 
slight  that  they  are  unmarked  by  the  organism  and  have  no  effect  upon 
it.  We  need  not  be  surprised,  therefore,  that  it  reacts  as  if  these  differ- 
ences did  not  exist ;  for  the  organism  they  do  not  exist. 

The  reaction  is  in  this  case  just  what  it  would  be  in  a  higher  organ- 
ism under  similar  conditions.  Let  us  suppose  that  the  light  stimulates 
strongly  the  sensitive  anterior  end,  the  eyes,  of  a  higher  animal  or  man  ; 
it  causes  pain  in  the  case  of  man.  There  will  be  a  tendency  (i)  to 
move  into  less  illuminated  regions  ;  (2)  to  turn  the  eyes  away  from  the 
light.  Suppose  that  the  man  is  enclosed  in  a  space  into  which  the 
sun  shines  obliquely  from  above,  and  that  the  end  from  which  it  shines 
is  a  little  less  illuminated  than  the  opposite  end,  owing  to  causes  similar 
to  those  in  Strasburger's  experiment  on  the  swarm-spores.  Suppose  that 
the  man  is  at  the  end  next  the  sun.  He  cannot  know  that  the  other 
end  is  more  illuminated,  for  the  only  way  this  would  be  possible  would 
be  for  the  greater  number  of  rays  of  light  to  meet  his  eye  coming  from 
that  direction,  while  by  hypothesis  all,  or  a  much  larger  number,  of 
the  rays  are  coming  from  the  opposite  direction.  He  will,  therefore, 
turn  his  eyes  away  from  the  sun,  and  if  he  moves  will  move  toward 
the  end  away  from  the  sun.  After  having  traversed  some  distance  he 
may  observe,  if  he  is  very  discriminating,  that  he  is  as  a  matter  of  fact 
getting  into  a  region  of  somewhat  greater  illumination,  and  may  perhaps 
reason  that  the  best  thing  he  can  do  under  the  circumstances  is  to  keep 
his  eyes  turned  away  from  the  source  of  light  and  move  backward  to  the 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  69 

less  illuminated  end.  But  this  involves  the  capability  of  making  fine 
distinctions,  and  a  considerable  degree  of  intelligence  in  deciding  what  to 
do  under  the  peculiar  circumstances.  The  experiment  with  the  swarm- 
spores  shows  that  they  are  incapable  of  such  fine  discrimination,  or  that 
they  are  not  sufficiently  intelligent  to  know  what  to  do  under  the  circum- 
stances. They  give  no  indication  that  they  notice  the  greater  illumina- 
tion after  having  passed  to  the  end  away  from  the  light.  Their  action 
may  be  considered  perhaps  in  a  certain  sense  as  a  "  mistake,"  but  it 
is  a  mistake  which  even  the  highest  organism  would  make,  and  which 
could  be  corrected  only  after  experience  of  its  results. 

The  results  of  our  study  of  the  light  reaction  in  ciliates  and  flagel- 
lates lead  to  conclusions  which  stand  in  sharp  contrast  with  certain 
general  conclusions  in  Radl's  recent  extensive  and  interesting  paper  on 
Phototropism  (Radl,  1903).  Radl  reaches  the  somewhat  extraordinary 
conclusion  that  light  orients  organisms  by  exercising  an  actual 
mechanical  pressure  upon  them.  This  pressure  necessarily  disturbs 
the  equilibrium  of  the  body,  which  is  then  compelled  to  change  posi- 
tion until  equilibrium  is  restored  ;  the  organism  is  then  oriented.  The 
orientation  is  a  consequence  of  the  interplay  of  two  sets  of  forces,  inner 
and  outer ;  these  cannot  be  in  equilibrium  until  the  body  has  taken  a 
certain  position  with  reference  to  the  pressure  exercised  by  the  light 
(/.  c,  pp.  151  fT.)  The  actual  turning  which  induces  orientation  must 
be  due  to  the  action  of  a  pair  of  forces  (/.  ^.,  p.  14^).  One  of  these 
forces  is  the  pressure  produced  by  the  light. 

Orientation  produced  in  the  manner  described  in  the  present  paper 
for  the  reaction  of  ciliates  and  flagellates  to  light,  and  in  the  preceding 
paper  for  the  reaction  to  heat,  could  of  course  not  be  brought  about  in 
the  manner  supposed  by  Radl.  One  of  Radl's  chief  arguments  for  his 
view  is  that  "no  observation  thus  far  shows  that  the  final  orientation 
is  attained  by  a  trial  or  after  an  oscillation,  but  it  takes  place  auto- 
matically"* (/.  c,  p.  141). 

The  observations  on  ciliates  and  flagellates  given  in  the  present  paper 
show  conclusively  that  the  orientation  in  these  cases  is  brought  about 
through  repeated  trials.  In  the  statement  quoted  above  Radl  has  over- 
looked certain  other  cases.  Thus  Strasburger,  as  we  have  seen  (p.  59), 
states  that  after  the  direction  of  the  light  is  changed  Hsematococcus 
becomes  reoriented  "  nach  verschiedenen  Schwankungen"  (Strasbur- 
ger, 1878,  p.  24).  Radl  himself  refers  on  a  previous  page  (p.  100)  to 
Strasburger's  observation  of  the  oscillating  movement  of  swarm-spores 
under  the  influence  of  a  variation  in  light  intensity;  Rothert  (1901, 


*"  Keine  bisherige  Beobachtung  zeigt  ferner,  dass  die  schliessliche  Orientie- 
rung  etwa  durch  eine  Priifung  oder  nach  einem  Schwanken  erzielt  wurde, 
sondern  sie  folgt  automatisch." 


70  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

p.  397)  has  called  particular  attention  to  this  as  a  possible  factor  in  the 
so-called  phototropism.  Radl  also  refers  (p.  99)  to  Exner's  view  that  in 
Copilia  the  movements  of  the  eyes  are  in  the  nature  of  a  trial  ("  abtasten  ") 
of  the  surroundings.  Radl's  statement,  quoted  above,  can  then  hardly 
be  considered  strictly  accurate,  even  leaving  out  of  consideration  the 
results  set  forth  in  the  present  paper.  In  many  organisms,  doubtless, 
the  reaction  to  light  is  of  that  direct  character  assumed  to  be  general  by 
Radl.  But  it  may  be  strongly  doubted  whether  this  is  what  we  may 
call  a  primitive  condition  ;  in  other  words,  whether  it  does  not  involve 
more  complicated  internal  processes  than  the  reaction  by  '*  trial  and 
error."  In  any  case,  I  am  convinced  that  a  similar  reaction  to  light  by 
the  method  of  "  trial  and  error  "  will  be  shown  to  exist  in  many  other 
organisms  ;  it  is  demonstrated,  for  example,  in  Rotifera,  in  the  paper 
which  follows  the  present  one. 

Recourse  will  doubtless  be  taken  to  the  usual  refuge  when  a  sharp 
concept  has  been  defined  to  which  the  phenomena  are  not  found  to 
correspond  ;  the  reactions  of  the  ciliates  and  flagellates  will  be  simply 
excluded  from  the  tropisms  and  the  definition  of  the  latter  maintained 
in  all  its  pristine  purity.  Indeed,  it  may  be  questioned  whether  the 
reactions  of  infusoria  (and  Rotatoria)  to  light  are  not  excluded  from 
phototropism  through  the  definition  given  by  Radl  on  p.  140,  what- 
ever the  method  by  which  they  are  produced.  Radl  says  "  Unter 
phototropischer  Orientierung  ist  die  Fahigkeit  der  Organismen  zu 
verstehen,  eine  feste  Einstellung  der  Achsen  des  gesamten  Korpers  in 
dem  Lichtfelde  einzunehmen."  Since  the  ciliate  or  flagellate  (or 
rotifer)  revolves  continually  on  its  long  axis,  and  swerves  continually 
toward  a  certain  side,  it  can  hardly  be  said  that  the  body  axes  have  a 
"  feste  Einstellung"  with  reference  to  the  light.  In  an  explanatory 
paragraph  Radl  says  that  in  orientation  "immer  geht  dann  der 
Lichtstrahl  durch  die  (morphologische)  Symmetrieebene  des  Korpers" 
(/.  c,  p.  140).  This  is  certainly  not  true  for  the  ciliate  or  flagellate  (or 
rotifer),  even  leaving  out  of  consideration  the  fact  that  in  the  former 
two  groups  the  animals  are  usually  unsymmetrical.  If  it  be  proposed, 
then,  to  exclude  the  light  reactions  of  ciliates,  flagellates,  and  rotifers 
from  the  concept  of  *'Phototropismus,"  one  can  only  agree  that  this  is 
necessary,  in  view  of  the  definitions  of  that  concept. 

But  what  is  the  value  of  a  definition  which  excludes  some  of  the  chief 
phenomena  on  which  the  concept  that  we  are  attempting  to  define  is 
based  .'*  And  what  is  the  value  of  a  theory  that  depends  on  such  a 
definition  and  that  can  only  be  correct  so  long  as  we  hold  to  this 
definition.?  The  phenomena  themselves  are,  after  all,  the  final  refer- 
ence for  testing  the  correctness  of  any  definition  or  theory ;  it  is  the 
observed  phenomena  that  we  are  attempting  to  formulate  and  explain. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  7 1 

What  we  desire  in  the  study  of  animal  behavior  is  (i)  a  correct 
description  of  what  occurs ;  (2)  an  understanding  of  the  relation  of 
what  occurs  here  to  other  phenomena,  this  constituting  their  "explana- 
tion" so  far  as  an  explanation  is  possible.  Whether  the  phenomena 
when  correctly  described  and  understood  are  found  to  fall  under  some- 
one's definition  of  a  tropism  is  comparatively  unimportant ;  it  is  only 
after  such  correct  description  and  understanding  that  final  definitions 
can  be  made.  I  question  much  if  there  has  not  been  undue  haste  in 
framing  precise  definitions  for  the  phenomena  of  animal  behavior,  when 
we  know  so  little  about  the  phenomena  in  any  thorough  way.  Radl, 
I  believe,  makes  a  fundamental  error  in  attempting  to  separate  "  Pho- 
totropismus"  rigidly  from  other  reactions  to  light.  Thus,  he  repeat- 
edly cites  Euglena  as  an  example  of  an  organism  that  shows  undoubted 
phototropism.  On  page  114  he  further  cites  the  motor  reaction  of 
Euglena  when  suddenly  shaded  *  as  a  reaction  that  has  nothing  to  do 
with  phototropism.  As  I  have  shown  above,  the  two  are  really 
closely  bound  up  together ;  the  orientation  in  the  "phototropism"  is 
produced  through  this  motor  reaction.  When  the  reactions  of  organ- 
isms to  light  are  known  in  detail,  I  believe  that  many  other  reactions 
which  Radl  (p.  1 14)  attempts  to  separate  sharply  from  "  phototropism  " 
will  be  found  closely  connected  with  the  reactions  that  go  under  that 
name.  I  had  occasion  to  point  out,  in  the  paper  preceding  this,  on 
the  reactions  to  heat,  that  if  everything  which  the  organisms  do,  except 
the  orientation  itself,  is  left  out  of  consideration,  the  orientation  can  be 
accounted  for  by  any  theory  desired.  A  thorough  study  of  precisely  this 
point — the  relation  of  "phototropism"  to  the  phenomena  supposedly 
unconnected  with  it — would,  I  believe,  have  saved  Radl  from  marring 
his  otherwise  most  excellent  and  useful  contribution  to  the  study  of 
light  reactions  by  the  proposal  of  so  fantastic  a  theory  to  account  for 
the  reactions  to  light ;  a  theory  that  fiiirly  produces  a  shock  in  the  mind 
of  the  reader  when  it  is  reached,  coming  as  it  does  after  Radl's  thorough 
and  valuable  objective  study  of  many  of  the  phenomena  and  his  exceed- 
ingly sane,  if  somewhat  sharp,  criticism  of  other  theories.  Definition 
and  precise  classification  are  of  course  valuable  at  a  certain  stage  of 
knowledge,  but  when  carried  out  without  a  thorough  knowledge  of  the 
phenomena  dealt  with  they  may  be  a  hindrance  rather  than  a  help. 
The  thorough  knowledge  of  the  phenomena  of  animal  behavior  required 
for  this  is  far  from  existing  at  present. 

♦Radl  says  when  "  beleuchtet";  this  is  evidently  a  slip  of  the  pen. 


THIRD    PAPER 


REACTIONS  TO  STIMULI  IN  CERTAIN 
ROTIFERA. 


73 


REACTIONS  TO  STIMULI  IN  CERTAIN   ROTIFERA. 


In  my  series  of ''Studies  on  Reactions  to  Stimuli  in  Unicellular 
Organisms  "  and  in  the  foregoing  papers  I  have  set  forth  the  reaction 
methods  of  many  infusoria  to  varied  stimuli.  The  result  has  been 
to  show  that  the  reaction  method  in  these  organisms  is  of  a  peculiar 
character,  differing  radically  from  that  required  by  prevailing  theories 
of  the  reactions  of  lower  organisms.  The  essential  nature  of  these 
reactions,  with  their  implications  as  to  the  character  of  behavior  in  the 
lower  organisms,  will  be  discussed  in  the  following  papers.  Before 
proceeding  to  this  discussion  it  is  important  to  determine  whether  the 
reaction  method  in  the  Infusoria  differs  radically  in  character  from 
that  of  Metazoa.  For  this  purpose  it  seems  well  to  select  a  group  of 
Metazoa  whose  habitat  and  mode  of  life  are  similar  to  those  of  the 
Infusoria.  In  this  way  differences  due  primarily  to  the  different  plan 
of  structure  of  the  two  sets  of  organisms  may  perhaps  be  brought  out 
without  the  complications  arising  from  different  modes  of  life. 

A  group  of  Metazoa  much  resembling  the  Infusoria  in  their  mode 
of  life  is  found  in  the  Rotatoria.  As  is  well  known,  the  members 
of  these  two  groups  are  usually  found  mingled  together.  They  are 
of  about  the  same  size,  and  both  swim  about  by  means  of  cilia.  So 
great  is  the  resemblance  in  general  habit  and  in  habitat  that  they  were 
at  first  classed  together,  all  being  given  the  name  of  Infusoria.  As 
we  know  now,  however,  they  are  really  widely  separated  in  relation- 
ship. While  the  Infusoria  are  unicellular,  the  Rotifera  are  multicellu- 
lar organisms  of  a  high  degree  of  complexity,  possessing  many  systems 
of  organs,  each  composed  of  many  cells.  In  particular,  they  have  a 
well-developed  nervous  system. 

A  comparison  of  the  behavior  of  these  two  groups  of  organisms 
should  show  us,  therefore,  whether  there  are  types  of  reaction  having 
a  high  degree  of  generality,  such  as  is  claimed  for  the  theory  of 
tropisms — types  that  may  give  a  key  to  the  behavior  of  groups  so 
widely  separated  in  relationship  as  the  two  under  consideration,  which 
are  representatives  of  the  Protozoa  and  of  Metazoa  of  a  fairly  high 
degree  of  organization. 

In  the  present  paper  I  can  attempt  to  give  an  account  of  the  behavior 
of  only  a  few  free-swimming  species,  and  that  not  in  an  exhaustive 
manner.  I  hope  to  return  to  an  extensive  study  of  the  behavior  of  this 
interesting  group,  so   as  to  develop  its  implications  for  the  theory  of 

75 


76 


THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


animal  behavior  in  general.     In  the  study  here  set  forth  observation 
"^-^^  was  directed  primarily  to  the  questions  of  howr 

certain  Rotifera  react  under  the  stimulus  of 
^  the  agencies  which  usualh'  give  rise  to  the  so- 
called  tropisms — light,  chemicals,  heat,  elec- 
tricity, contact,  etc. — and  to  these  questions 
the  present  account  will  be  devoted. 

The  species  whose  reactions  were  exam- 
ined belong  chiefly  to  the  loricate  group  of 
free-swimming  Rotifera,  and  include  a  num- 
ber of  species  of  the  Rattulidae,  several  species 
of  Cathypnadae,  two  or  three  species  of  Euch- 
lanis,  Plcesoma  lenticular e^  Anurcea  cochle- 
ar is  ^  and  Brachionus  pala.  These  were 
studied  as  opportunity  offered.  In  most  cases 
the  reactions  of  any  one  species  were  not 
determined  with  relation  to  more  than  two 
or  three  classes  of  stimuli.  The  behavior  of 
Anurcea  cochlear  is  was  examined  most  fully. 
This  species  will  be  used  as  a  type  in  describ- 
ing the  reactions.  I  have  already  given  a 
brief  account  of  the  general  reaction  type  in 
certain  species  of  the  Rattulidag  in  my  mono- 
graph of  that  group  (Jennings,  1903). 

METHOD  OF  LOCOMOTION. 

The   free-swimming   Rotifera   progress 

through  the  water  in  the  same  manner  as  the 

ciliate  infusoria.     The   cilia  in  the  Rotifera 

are  limited  to  the  anterior  end,  as  they  are 

in  the  peritrichous  infusoria.     It  is  interesting 

to  note  that  the  same  device  is  adopted  in  the 

one  group  as  in  the  other,  to  compensate  for 

irregularities  in  the  form  of  the  body,  etc., 

Fig.  25.*  which    might   result   in    swerving   from    the 

straight  course.     This  is  by  revolution  on  the  long  axis,  causing  the 

path  to  become  a  spiral  with  a  straight  axis.     In  the  Infusoria  the 


*  Fig.  25. — Spiral  path  followed  in  ordinary  swimming  by  Anuria  cochlearis 
Gosse,  showing  different  positions  of  body  in  different  parts  of  the  course; 
a,  dorsal  surface;  3,  left  side;  c,  ventral  surface;  d,  right  side.  The  animal 
revolves  on  its  long  axis  over  to  the  right,  thus  taking  successively  the  positions 
«,  *,  c,  </,  a,  etc.  The  large  arrow  indicates  the  general  direction  of  the  course 
followed;  the  smaller  arrows  show  direction  of  progression  in  certain  parts  of 
the  course. 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA.  77 

organism  usually  swerves  from  the  straight  line  toward  the  aboral  side  ; 

in  the  Rotatoria  it  is  usually  toward  the  dorsal  side.  Well-ordered 
forward  progression  would  therefore  not  take  place,  were  it  not  for  the 
revolution  on  the  long  axis,  converting  the  circular  course  into  a  spiral 
one.  In  the  Rotifera  the  revolution  on  the  long  axis  is,  so  far  as 
observed,  always  over  to  the  right.  These  relations  have  been  brought 
out  in  detail  in  a  previous  paper  by  the  present  author  (Jennings,  1901). 
The  spiral  path  thus  followed  by  most  of  the  free-swimming  Roti- 
fera may  be  illustrated  in  Fig.  25,  for  Anurcea  cochlear  is  Gosse.  As 
will  be  seen  from  the  figure,  the  path  followed  depends  upon  three 
factors  :  (i)  the  animal  continually  swerves  toward  its  dorsal  side  ;  (2) 
it  progresses  ;  (3)  it  revolves  on  its  long  axis.  The  result  of  these  three 
factors  is  the  spiral  course.  In  all  these  relations  the  rotifer  agrees 
with  the  infusorian. 

REACTIONS  TO  STIMULI. 

The  most  general  reaction  to  a  stimulus  in  such  a  free-swimming 
rotifer  is  an  accentuation  of  one  of  the  factors  in  this  course,  namely, 
the  swerving  toward  the  dorsal  side.  The  result  is  to  produce  a  spiral 
of  much  greater  width  than  previously  existed.  This  may  often  be 
observed  when  the  vessel  containing  the  rotifers  is  jarred.  It  is  evi- 
dent that  this  method  of  reaction  is  fitted  to  enable  the  rotifer  to  avoid 
a  small  obstacle  lying  in  its  path,  that  is,  in  the  axis  of  the  spiral. 
When  the  animal  resumes  its  former  method  of  swimming  the  axis  of 
the  spiral  lies  in  a  new  direction  ;  the  course  has  thus  been  slightly 
changed. 

With  a  stronger  stimulus,  as  when  the  rotifer  strikes  against  an 
object  lying  in  its  path,  the  swerving  toward  the  dorsal  side  may  be 
still  more  pronounced,  while  the  revolution  on  the  long  axis  nearly  or 
quite  ceases.  The  result  is  that  the  organism  swings  strongly  toward 
its  dorsal  side,  and  when  the  usual  forward  swimming  is  resumed  the 
axis  of  the  spiral  lies  in  a  totally  new  direction  (Fig.  26).  It  thus 
avoids  the  obstacle,  if  the  latter  is  small ;  if  the  first  reaction  does  not 
avoid  the  obstacle  completely  the  reaction  is  repeated  until  the  course 
is  sufiiciently  altered  so  that  the  rotifer  no  longer  strikes  against  the 
source  of  stimulus.  In  some  rotifers  the  increased  swerving  toward 
the  dorsal  side  is  preceded  by  swimming  backward  a  short  stretch. 

In  all  these  points  the  reaction  of  the  rotifer  agrees  even  to  details 
with  that  of  the  ciliate  infusorian.  There  is  a  difference  in  the  fact 
that  the  Infusoria  are  unsymmetrical  and  cannot  therefore  be  said  to 
swerve  toward  the  dorsal  side,  as  do  the  prevailingly  symmetrical 
Rotifera.  In  the  Rattulidas,  however,  we  have  asymmetry  of  a  char- 
acter similar  to  that  found  in  the  Infusoria. 


78 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


We  have  dealt  thus  far  specifically  only  with  reactions  to  simple 
mechanical  stimuli,  such  as  are  presented  by  an  obstacle  in  the  path  of 


Fig.  26.* 


the  rotifer  or  by  a  simple  mechanical  jar.     This  type  of  reaction  under 
such  conditions  I  have  observed  for  Dlurella  tigris  Miiller,  D.  por- 


*  Fig.  26  is  a  diagram  of  the  reaction  of  the  rotifer  Anuraea  to  a  strong  stimulus, 
as  when  it  reaches  a  source  of  mechanical  stimulus  or  a  region  where  some 
chemical  is  dissolved  in  the  water.  From  a  to  b  the  animal  is  unstimulated, 
hence  it  follows  the  usual  spiral  course.  At  b  it  reaches  the  stimulating  region, 
whereupon  it  turns  strongly  toward  the  dorsal  side,  following  the  arc  of  a  circle, 
from  b  to  d.  Here  it  resumes  the  usual  spiral  course  {d  to  e).  The  large  arrow 
M  shows  the  general  direction  of  progression  before  the  stimulus  was  received; 
the  arrowy'  shows  the  direction  of  progression  after  the  reaction  has  taken  place. 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


79 


cellus  Gosse,  D,  gracilis  Tessin,  and  a  number  of  other  species  of 
Rattulidae  ;  Plcesoma  lenticulare  Herrick,  Cathypna  ungulata  Gosse, 
Monostyla  bulla  Gosse,  Brachionus  pala  Ehr.,  Anurcea  cochlear  is 
Gosse,  and  A.  aculeata  Ehr. 

This  method  by  no  means  exhausts  the  possibilities  of  reaction  even 
to  a  simple  mechanical  stimulus  in  these  species.  They  may  retract 
the  head  and  cease  swimming,  may  creep  over  the  surface  of  the  object 
with  which  they  come  in  contact,  or  possibly  may  sometimes  turn  other- 
wise than  to  the  dorsal  side  when  stimulated.  Of  this  latter  point  I 
am,  however,  by  no  means  sure.  It  is  certain  that  the  typical  reaction, 
occurring  in  the  great  majority  of  cases,  is  that  described  above. 

REACTION  TO  CHEMICALS. 

The  reaction  given  when  the  organism  comes  in  contact  with  an  area 
containing  a  rather  strong 
diffusing  chemical  was 
observed  in  Metopidia 
lepadella^  Anurcea  coch- 
lear is  ^  A.  aculeata^  and 
Diurella  gracilis. 

The  method  of  experi- 
mentation was  as  follows : 
A  drop  of  water  contain- 
ing the  rotifers  was  placed 
on  a  slide.  Near  this  was 
placed  a  drop  of  N/8 
NaCl,  and  the  two  drops 
were  connected  by  a  nar- 
row neck.  The  behavior 
of  the  organisms  as  they 
came  into  the  region  of  the  neck  and  thus  in  contact  with  the  salt 
solution  was  observed  with  the  Braus-Driiner  microscope.  In  the 
species  mentioned  the  reaction  was  by  a  sudden  turn  toward  the  dorsal 
side,  by  which  the  path  of  the  animal  was  directed  away  from  the 
chemical.  The  reaction  is  thus  of  the  same  character  as  occurs  in  the 
ciliate  infusoria. 

This  manner  of  reaction  to  chemicals  is  in  both  these  groups  of 
organisms  just  what  might  be  expected  when  the  currents  caused  by 
the  cilia  are  taken  into  consideration.     In  the  ciliate,  as  I  have  shown 


Fig.  27.* 


♦Fig.  27.— Diagram  of  currents  in  a  nearly  quiet  Anuraea,  showing  how  a 
diffusing  chemical  or  an  advancing  region  of  warmer  water  (represented  by  shad- 
ing), is  drawn  out  by  the  ciliary  vortex,  so  as  to  reach  the  mouth  and  the  ventral 
surface  before  affecting  other  parts  of  body. 


8o  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

in  a  previous  paper  (Jennings,  1902,  a) ,  the  cilia  cause  a  current  coming 
from  the  region  in  front  of  the  organism  to  pass  along  the  oral  surface 
to  the  mouth  ;  in  this  way  the  oral  surface  comes  in  contact  with  the 
chemical  before  any  other  part  is  afiected.  It  is  not  surprising,  there- 
fore, that  the  organism  should  turn  toward  the  opposite  (aboral)  side. 

In  the  rotifera  the  conditions  are  parallel  to  those  found  in  the  ciliate. 
The  cilia  cause  a  current,  which  passes  to  the  mouth,  on  the  ventral 
surface  of  the  body  (Fig.  27) .  The  solution  thus  reaches  the  ventral 
surface  first,  and  the  reaction  is,  as  might  be  expected,  a  turn  toward 
the  dorsal  side. 

It  should  be  distinctly  stated  that  this  reaction  method  is  not  universal 
in  rotifers  even  toward  chemical  stimuli.  In  some  of  the  larger  species, 
bearing  auricles,  or  with  the  ciliary  apparatus  of  a  very  complex 
character  in  other  respects,  varied  reactions  may  occur,  which  I  hope 
to  analyze  in  another  paper. 

REACTION  TO  HEAT. 

This  was  studied  in  detail  only  in  Anurcea  cochlearis.  A  large 
number  of  the  rotifers  were  mounted  in  a  shallow  trough  formed  of  a 
slide,  as  described  on  p.  12,  and  one  end  of  the  slide  was  warmed  by 
means  of  the  apparatus  shown  in  Fig.  5.  The  reactions  were  then 
observed  with  the  Braus-Driiner  stereoscopic  binocular. 

As  soon  as  a  portion  of  the  slide  has  been  warmed  above  the  optimum, 
the  rotifers  in  this  region  turn  more  strongly  than  usual  toward  the 
dorsal  side,  so  that  the  course  followed  becomes  a  very  wide  spiral  and 
the  animals  make  little  progress.  If  the  heat  is  increased  the  revolu- 
tion on  the  long  axis  ceases,  while  the  animals  swerve  still  more 
strongly  toward  the  dorsal  side  (Fig.  28),  so  that  they  swim  in  circles, 
the  dorsal  surface  being  directed  toward  the  center  of  the  circle. 
Usually  after  circling  thus  a  short  time  the  animals  begin  again  to  re- 
volve on  the  long  axis,  and  dart  forward.  The  direction  of  this  dart 
forward  seems  purely  random.  If  it  carries  the  animal  out  of  the 
heated  region  the  forward  movement  is  continued  and  the  animal 
escapes.  If  it  does  not  carry  the  animal  out  of  the  heated  region  the 
circling  toward  the  dorsal  side  is  quickly  resumed,  followed  by  another 
dart  forward.  This  is  continued  either  until  the  rotifer  passes  out  of 
the  heated  region  or  until  it  is  overcome  by  the  heat.  Usually,  if  it 
does  not  escape  soon  from  the  heated  region  the  circling  becomes 
more  rapid  and  continuous  and  is  kept  up  till  the  animal  is  destroyed 
by  the  heat. 

If  one  end  of  the  slide  is  heated  and  the  animal  approaches  the 
heated  region  from  the  opposite  end  the  reaction  is  of  the  same 
character  as  that  last  described.     As  soon  as  the  region  is  reached 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


8l 


where  the  heat  acts  as  an  effective  stimulus  the  animal  swerves  strongly 
toward  the  dorsal  side,  thus  beginning  to  circle,  as  shown  in  Fig.  28. 
If  this  swerving  should  continue  only  till  the  animal  had  described  a 
semicircle,  then  were  followed  by  the  forward  dart,  the  animal  would 
of  course  retrace  its  original  course  (or  one  parallel  to  it) ,  and  would 
thus  escape  from  the  heated  region,  as  happens  in  the  reaction  to  the 
electric  current  (Fig.  29) .    But  the  reaction  to  heat  is  less  precise  than 

f 


Fig.  28. 


this.  ■  Usually  the  animal  makes  several  com- 
plete circles  before  darting  forward,  and  the 
direction  in  which  it  darts  seems  a  random 
one  ;  sometimes  it  is  toward  the  heated  region, 
sometimes  away  from  it,  sometimes  oblique  to 
it.  If  the  path  followed  leads  the  animal  into 
the  heated  region  the  circling  toward  the  dorsal 
side,  followed  by  the  dart  forward,  is  repeated  ;  while  if  the  path  leads 
away  from  the  heat  no  farther  reaction  is  caused  and  the  animal  escapes. 
Thus  when  a  large  number  of  the  animals  swim  toward  the  heated 
region  a  considerable  number  will  be  seen  a  little  later  to  swim  away 
again.  But  in  many  cases  the  dart  forward  carries  the  animal  still 
farther  into  the  heated  region.  These  specimens  then  begin  to  circle 
again  toward  the  dorsal  side,  and  if  the  temperature  is  high  they  may 


♦Fig.  28. — Diagram  of  a  reaction  to  heat  in  Anuraea.  The  unstimulated 
animal  at  first  advances  in  the  general  direction  shown  by  the  arrow  x,  following 
thus  the  course  a  to  e.  The  heat  is  supposed  to  be  advancing  from  the  direction 
opposite  the  arrow  x.  When  the  rotifer  reaches  the  point  e  the  heat  becomes 
effective  as  a  stimulus.  The  animal  reacts  by  turning  toward  the  dorsal  side, 
and  continues  this  so  as  to  describe  a  complete  circle,/",  g;  A,  /',/",  etc. ;  often  it 
describes  such  a  circle  several  times.  Finally,  at  some  point  in  the  circular 
course,  as  £-,  it  resumes  the  usual  spiral  course,  following  thus  the  path  ^, /,  /. 
Its  original  course,  shown  by  the  arrow  x,  has  thus  been  exchanged  for  a  course 
having  the  general  direction  shown  by  the  arrow  v. 


82  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

continue  this  till  death  intervenes.  In  many  cases  they  repeat  the  dart 
forward  and  some  escape  in  this  way,  while  others  do  not. 

The  reaction  of  Anuraea  to  heat  is,  therefore,  not  very  precise,  and 
many  individuals  swim  into  the  heated  region  and  are  killed.  Those 
which  escape  do  so  through  a  reaction  which  is  similar  to  that  of 
those  which  do  not ;  in  the  one  case  the  forward  movement  carries  the 
animal  out  of  the  heated  region  ;  in  the  other  it  does  not.  The  essential 
point  to  the  reaction  is  that  the  animals  when  stimulated  by  heat  change 
their  course  (through  a  ''  motor  reflex").  This  changed  course  nat- 
urally is  an  advantage,  and  in  accordance  with  the  laws  of  probability 
carries  some  of  the  organisms  away  from  the  source  of  danger.  Others, 
likewise  in  accordance  with  the  laws  of  probability,  are  carried  even 
by  the  changed  course  toward  the  heated  region,  where  they  may  be 
killed  unless  a  repetition  of  the  "motor  reflex"  with  its  change  of 
course  carries  them  finally  away.  The  reaction  is  by  the  method 
of"  trial  and  error,"  and  is  not  always  successful. 

Altogether,  the  reaction  of  the  rotifer  Anursea  to  heat  is  of  a  charac- 
ter similar  in  principle  to  that  of  Oxytricha  (Fig.  7,  p.  16).  The 
direction  of  turning  depends  on  an  internal  factor ;  the  reaction  takes 
the  form  of  "  a  motor  reflex,"  and  is  by  no  means  compatible  with  the 
typical  tropism  schema. 

REACTION  TO  LIGHT. 

In  light,  as  I  have  already  set  forth  in  the  account  of  the  reactions  of 
Stentor,  we  have  a  stimulating  agent  of  a  different  character  from  that 
found  in  chemicals  or  in  heat,  since  the  distribution  of  the  stimulating 
agent  is  not  affected  by  the  currents  of  water  produced  by  the  motor 
organs  of  the  animal.  There  is  thus  no  reason  in  the  distribution  of 
the  stimulating  agent  to  favor  a  turning  toward  one  side  rather  than  the 
other. 

I  have  been  able  to  study  accurately  the  light  reaction  in  but  one 
rotifer,  Anurcea  cochlearis  Gosse.  The  conditions  necessary  for 
precise  observation  of  the  nature  of  the  reaction  are  very  difficult  to 
fulfill,  and  the  usual  movements  of  the  animals  are  such  that  the  nature 
of  the  reaction  is  obscured.  As  will  be  recalled,  the  organism  is 
normally  swimming  rapidly  in  a  spiral,  continually  swerving  toward 
its  dorsal  side.  This  in  itself  is  very  confusing  when  one  attempts  to 
observe  just  how  the  organism  turns  when  stimulated.  When  light  is 
thrown  upon  it,  or  when  the  direction  of  light  falling  on  it  is  changed, 
the  response  is  usually  not  given  at  once,  and  when  it  does  occur,  as 
we  shall  see,  it  may  be  in  the  form  of  an  accentuation  of  certain  features 
of  the  normal  movement.  From  these  conditions  it  results  that  it  is 
exceedingly  difficult  to  tell,  after  a  reaction  to  light  has  clearly  occurred, 


REACTIONS    TO    STIMULI    IN    CERTAIN    KOTIFERA.  S3 

just  how  the  reaction  took  place.  Of  course,  only  sharply  defined  posi- 
tive observations  are  of  value  in  deciding  between  two  opposing  possi- 
bilities ;  hence,  although  I  have  studied  a  number  of  other  rotifers  in 
this  connection,  I  give  the  results  only  where  absolutely  sure  of  them. 
But  in  the  two  or  three  other  rotifers  I  have  examined  in  this  connection 
the  reaction  is  apparently  the  same  as  that  in  AnurcEa  cochlearis^  to 
be  described  at  once. 

The  specimens  of  Anurcea  cochlearis  studied  had  been  in  a  small 
aquarium  in  the  laboratory  some  months,  and  were  distinctly  negative 
to  light,  gathering  at  the  side  of  vessel  farthest  from  the  window.  The 
freshly  collected  animals  are,  I  believe,  usually  positive  to  light. 

These  negative  individuals  were  placed  in  a  small  flat-bottomed 
rectangular  glass  vessel,  on  a  dark  background,  in  a  dark  room.  At 
opposite  sides  of  the  vessel  and  somewhat  above  were  clamped  two 
incandescent  electric  lights,  A  and  B^  at  a  distance  of  about  lo  inches* 
in  the  manner  described  for  Stentor  (p.  41  and  Fig.  15).  One  of 
these  lights  could  be  extinguished  while  the  other  was  simultaneously 
turned  on.  In  this  way  the  direction  of  the  light  falling  on  the  rotifers 
could  be  reversed. 

When  only  one  of  the  lights,  as  A^  was  turned  on,  the  Anuraeas  all 
collected  at  the  opposite  side  of  the  vessel,  next  to  B.  When  A  was 
extinguished  and  B  turned  on,  they  turned  and  swam  in  the  opposite 
direction,  toward  A.  By  reversing  the  direction  of  the  light  while  the 
animals  were  crossing  the  vessel  their  course  could  be  reversed  while 
in  full  career. 

Focusing  the  Braus-Driiner  on  the  vessel,  and  reversing  the  lights 
when  the  animals  were  well  in  the  field  of  observation,  the  following 
could  be  observed :  Some  turned  at  once,  with  some  sharpness, 
toward  the  dorsal  side^  the  turning  continuing  until  the  direction  of 
swimming  was  reversed  and  the  animals  were  again  swimming  away 
from  the  light  (Fig.  29) .  In  these  cases  the  direction  of  turning  was 
clear  and  could  be  observed  without  great  difficulty. 

Other  individuals  continued  for  a  short  time  to  swim  in  the  same 
direction  as  before,  then  turned,  either  sharply,  as  just  described,  or 
more  slowly,  in  the  manner  to  be  described. 

Where  the  turning  was  sharp,  as  described  above,  there  was  no 
great  difficulty  in  determining  with  certainty  the  nature  of  the  reaction. 
But  in  many  cases  the  turning  took  place  more  slowly,  in  the  following 
manner :  Either  as  soon  as  the  light  was  reversed,  or  very  soon  after, 
the  width  of  the  spiral  in  which  the  animal  was  swimming  became 
much  greater.  In  other  words,  the  animal  swerved  more  toward  the 
dorsal  side  and  progressed  less  rapidly  than  usual.  Thus  it  described 
rather  wide  circles,  and  the  swerving  toward  the  dorsal  side  increased, 


84  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

while  progression  and  revolution  on  the  long  axis  had  largely  ceased. 
After  this  circling  had  continued  for  some  time,  the  swerving  toward 
the  dorsal  side  apparently  continually  increasing,  it  was  found  that  the 
anterior  end  was  directed  away  from  the  source  of  light;  /.  e.^  the 
direction  of  swimming  had  been  reversed,  and  the  animal  was  moving 
away  from  the  light. 

It  is  obviously  very  difficult  to  be  entirely  certain  of  all  that  has  hap- 
pened during  this  period  of  extensive  circling,  as  a  matter  of  direct 
observation.  But  the  evidence  seems  to  show  clearly  that  the  essential 
point  in  changing  the  course  is  the  swerving  toward  the  dorsal  side. 
The  following  facts  all  point  to  this  conclusion  :  (i)  In  the  individuals 
which  turn  at  once  it  is  possible  to  be  entirely  certain  that  the  turning 
is  toward  the  dorsal  side.  (3)  In  the  individuals  which  are  circling  it 
is  entirely  clear  that  the  swerving  toward  the  dorsal  side  is  greatly  in- 
creased, and  there  is  no  evidence  of  turning  in  other  directions.  The 
only  difficulty  is  that  one  cannot  follow  every  evolution  and  be  certain 
that  nothing  else  has  occurred.  (3)  Analysis  of  this  same  reaction 
when  given  in  response  to  other  stimuli,  where  the  conditions  are 
more  favorable  for  observation,  shows  that  it  does  consist  of  an  in- 
creased swerving  toward  the  dorsal  side,  with  a  decrease,  or  an  entire 
stoppage  for  a  time,  of  the  forward  motion.  There  is,  then,  no  reason 
to  think  that  the  reaction  contains  other  factors  when  performed  under 
the  influence  of  light.  The  reaction  is  indeed  clearly  the  same  as  that 
described  for  Euglena  on  p.  53,  and  illustrated  in  Fig.  21  ;  a  similar 
analysis  could  be  given  for  the  reaction  of  Anuraea. 

It  may  be  considered  certain,  therefore,  that  in  Anurcea  cochlearis 
the  reaction  to  light  is  similar  to  the  reaction  to  other  stimuli,  and  that 
the  orientation  is  brought  about  by  a  turning  toward  the  dorsal  side. 
The  reaction  is,  therefore,  not  due  to  the  direct  effect  of  the  light  on  the 
motor  organs ;  the  direction  of  turning  is  determined  not  by  external 
factors,  but  by  internal  factors.  The  reaction  to  light  in  the  rotifer, 
like  that  in  the  infusorian,  takes  place  by  the  method  of  "  trial  and 
error." 

REACTION  TO  THE  ELECTRIC  CURRENT. 

A  considerable  number  of  different  species  of  the  rotifera  were  sub- 
jected to  the  continuous  electric  current  without  the  production  of  any 
characteristic  reaction.  A  current  was  used  which  could  be  graded  in 
strength  from  practically  zero  to  one  that  was  destructive,  but  no  reac- 
tion comparable  to  that  found  in  the  ciliate  infusoria  was  produced. 
On  making  or  breaking  the  current  the  animals  frequently  contracted 
quickly,  and  if  the  current  was  very  strong,  the  head  was  completely 
retracted  and  the  animal  sank  to  the  bottom.  But  there  was  no  orien- 
tation  and   the  animals  did  not  swim  toward  either  electrode.     These 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA.  85 

negative  results  were  obtained  with  several  of  the  Philodinadse  (Rotifer, 
Philodina),  some  species  of  Euchlanis  and  Salpina,  Noteus  quadri- 
cornis^  and  a  number  of  the  Rattulidas. 

In  Hydatina  senta  there  is  a  reaction  of  a  peculiar  character  which 
perhaps  furnishes  a  clue  to  the  cause  of  the  more  pronounced  reaction 
to  be  described  for  Anuraea.  With  a  current  of  moderate  strength, 
such  as  that  to  which  Paramecia  react  most  markedly,  Hydatina  shows 
no  reaction  except  when  the  head  is  directed  toward  the  anode.  But 
in  this  position  the  animal  at  once  retracts  its  cilia  and  sinks  to  the 
bottom.  Thus  a  Hydatina  may  swim  freely  about  in  water  through 
which  the  current  is  passing,  provided  it  swims  toward  the  cathode,  or 
transversely,  or  obliquely  ;  as  soon,  however,  as  it  turns  its  head  toward 
the  anode  it  stops  swimming  and  sinks  to  the  bottom.  Thus  if  an 
electric  current  is  passed  through  a  preparation  containing  a  large 
number  of  specimens  of  Hydatina,  many  will  be  seen  swimining 
toward  the  cathode  and  others  at  all  sorts  of  angles  with  the  current,  but 
none  toward  the  anode.  This  is  a  phenomenon  akin  to  what  I  have 
elsewhere  called  the  production  of  orientation  by  exclusion.  If  organ- 
isms are  prevented  from  swimming  in  any  direction  but  one,  after  a 
time,  provided  the  course  is  frequently  changed,  all  that  are  swim- 
ming will  be  found  moving  in  that  one  direction.  This  condition  is 
realized,  as  I  have  shown  in  the  first  of  these  contributions,  in  the 
reactions  of  infusoria  to  heat  and  cold.  But  in  the  reactions  of  Hydatina 
to  the  electric  current  the  "  exclusion"  is  less  complete  than  in  the 
cases  just  mentioned ;  the  animal  may  swim  in  any  direction  except 
one. 

The  fact  that  the  head  is  retracted  when  directed  toward  the  anode 
and  not  in  other  positions  indicates  that  there  is  a  greater  stimulation 
at  the  anode  than  elsewhere.  This  agrees  with  much  that  is  seen  in 
the  reactions  of  infusoria  to  the  current.  After  Hydatina  has  sunk  to 
the  bottom  with  anterior  end  to  the  anode,  it  repeatedly  makes  attempts 
to  unfold  its  cilia.  But  scarcely  have  they  begun  to  operate  when 
they  are  withdrawn  again.  Each  time  that  they  are  uncovered  for  an 
instant,  however,  they  turn  the  animal  a  little  toward  its  dorsal  side. 
Thus,  after  a  considerable  number  of  attempts  to  unfold  the  cilia,  the 
head  has  become  turned  away  from  the  anode  ;  then  the  cilia  are  spread 
out  and  the  animal  goes  on  its  way  until  it  is  so  incautious  as  to  turn 
its  head  again  toward  the  anode. 

Anurcea  cochlearis  shows  marked  electrotaxis  similar  to  that  found 
in  the  infusoria.  When  the  continuous  current  is  passed  through  a 
preparation  containing  large  numbers  of  this  species,  all  orient  quickly 
and  swim  toward  the  cathode.  They  thus  agree,  so  far,  in  their 
reaction  to  the  electric  current,  with  the  ciliate  infusoria. 


86  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  question  as  to  the  mechanism  of  the  electrotactic  reaction  in  the 
rotifer  is  of  interest  when  one  compares  the  structure  of  these  animals 
with  that  of  the  ciliate  infusoria.  The  Rotifera,  in  place  of  having  cilia 
scattered  over  the  entire  body,  are  furnished  only  with  a  group  of 
cilia  at  the  anterior  end.  In  the  Ciliata  it  is  usually  possible  to  distin- 
guish functionally  two  groups  of  cilia  (i)  the  a  do  ral  cilia.,  about  the 
mouth  and  oral  groove,  or  at  the  anterior  end ;  (2)  the  body  cilia, 
scattered  over  the  body.  The  cilia  of  the  rotifers  correspond  function- 
ally with  the  adoral  cilia  of  the  Ciliata. 

Pearl  (1900),  Wallengren  (1902-1903),  and  others  have  shown  that 
in  the  electrotactic  reaction  of  the  ciliates  the  two  sets  of  cilia  are  in 
many  cases  from  a  functional  standpoint  differently  affected.  The 
adoral  cilia  react  under  the  influence  of  the  electric  current  in  such  a 
way  as  to  tend  to  turn  the  organism  toward  the  aboral  side ;  that  is, 
they  tend  to  produce  the  same  reaction  which  the  organism  gives  in 
response  to  most  other  stimuli,  a  reaction  not  in  harmony  with  the 
tropism  schema.  The  body  cilia,  on  the  other  hand,  are  differently 
affected  on  the  different  sides  or  ends  of  the  organism  ;  those  on  the 
part  of  the  body  directed  toward  the  cathode  striking  in  one  direction  ; 
those  on  the  part  directed  toward  the  anode  striking  in  a  different 
direction.  The  result  is  that  the  organism,  through  the  action  of  the 
body  cilia,  tends  to  become  directly  oriented  in  a  way  that  is  in  harmony 
with  the  tropism  schema.  (For  details,  see  the  papers  cited.)  In  those 
ciliates  in  which  the  body  cilia  are  much  reduced,  as  in  the  Hypotricha, 
the  turning  is  determined  throughout  by  the  adoral  cilia,  so  that  the 
orientation  does  not  take  place  in  accordance  with  the  tropism  schema, 
while  in  some  others,  such  as  in  Paramecium,  the  influence  of  the  body 
cilia  is  predominant,  and  the  turning  is  in  accord  with  the  theory  of 
tropisms. 

What  conditions  shall  we  find  in  the  Rotifera,  where  the  only  exist- 
ing cilia  seem  to  agree  functionally  with  the  adoral  cilia  of  the  Ciliata? 

As  we  have  seen,  Anuraea  swims  as  a  rule  in  rather  wide  spirals, 
swerving  strongly  toward  the  dorsal  side  and  revolving  on  its  long  axis 
(Fig.  25).  When  the  electric  current  suddenly  acts  upon  it  the  organism 
at  once  turns  strongly  toward  the  dorsal  side,  continuing  the  turn  until 
its  head  is  brought  toward  the  cathode,  toward  which  it  swims  (Fig. 
29).  In  some  cases,  as  we  shall  see  later,  several  reactions  are  neces- 
sary for  bringing  the  body  in  line  with  the  current,  but  these  are  as  a 
rule  very  quickly  accomplished. 

If,  while  the  animals  are  swimming  toward  the  cathode,  the  current 
is  suddenly  reversed,  the  animals  again  turn  strongly  toward  the  dorsal 
side,  continuing  the  turning  until  their  position  is  reversed  and  the 
heads  point  toward  the  new  cathode  (Fig.  29).     In  many  cases  the 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


87 


turning  is  continued  still  farther,  so  that  the  head  of  the  animal  de- 
scribes a  complete  circle  ;  indeed,  this  may  continue  so  that  the  animal 
whirls  around  several  times,  always  towards  the  dorsal  side.  The 
reaction  thus  far  is  the  same  as  that  produced  by  heat  (Fig.  28).  In 
reacting  to  the  electric  current  the  whirling  finally  ceases  with  ante- 


FiG.  29.* 

rior  end  directed  toward  the  new  cathode.  The  animal  then  swims 
forward  in  the  direction  so  indicated.  These  turnings,  even  when 
several  times  repeated,  require  but  a  moment,  so  that  very  soon  prac- 
tically all  the  specimens  are  swimming  toward  the  new  cathode.     The 


*  Fig.  29. — Diagram  of  method  by  which  Anuraea  becomes  oriented  to  rays  of 
light,  or  to  the  electric  current.  Taking  the  latter  for  example,  the  animal  is  at 
first  swimming  toward  the  cathode,  in  direction  indicated  by  arrow  At;  it  thus 
follows  a  spiral  path  from  a  to  b.  At  b  the  electric  current  is  reversed.  The 
animal  thereupon  swerves  stronglj' toward  its  dorsal  side,  describing  a  semicircle, 
3,  c,  </,  until  its  anterior  end  is  directed  toward  the  new  cathode,  in  the  opposite 
direction  from  before.  It  now  follows  the  spiral  path  d  to  e.,  in  the  general  direc- 
tion indicated  by  the  arrowy'.  The  facts  are  similar  for  the  reversal  of  light,  or 
for  the  reaction  when  the  current  or  the  light  is  first  set  in  operation. 


S8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

reaction  in  AnuraBa  is  in  a  general   view  as  striking  and  clear-cut  as 
that  of  Paramecium. 

Thus  in  the  rotifer  Anurasa  the  orientation  to  the  continuous  elec- 
tric current  is  produced  through  a  motor  reaction,  the  essential  features 
of  which  are  determined  by  the  structure  of  the  organism.  The  organ- 
ism turns  always  toward  the  dorsal  side,  continuing  or  repeating  the 
turning  until  the  anterior  end  is  directed  toward  the  cathode.  In  these 
respects  it  agrees  with  hypotrichous  Ciliata,  where  the  direction  of 
turning  is  determined  by  the  action  of  the  adoral  cilia.  The  method 
of  reaction  is  quite  incompatible  with  the  tropism  schema. 

SUMMARY. 

The  reactions  of  those  Rotifera  of  which  an  account  is  given  in  this 
paper  take  place  in  a  manner  essentially  similar  to  the  reactions  of  the 
ciliate  infusoria. 

In  the  reactions  to  mechanical  stimuli,  to  chemicals,  and  to  heat, 
orientation  is  not  a  striking  feature.  The  organism  turns  when  stimu- 
lated toward  a  structurally  defined  side — as  a  rule  toward  the  dorsal 
side  ;  in  this  way  it  avoids  the  source  of  stimulus. 

In  the  negative  reaction  to  light  the  organism  becomes  oriented  with 
anterior  end  directed  away  from  the  source  of  strongest  light,  but  this 
orientation  is  brought  about  in  the  same  manner  as  in  Stentor ;  the 
animal  turns  toward  the  dorsal  side  without  relation  to  the  side  on 
which  the  light  strikes  it,  and  continues  the  turning  or  repeats  it  until 
the  anterior  end  is  directed  away  from  the  source  of  light. 

To  the  continuous  electric  current  the  rotifer  Anuraea  orients  and 
swims  directly  toward  the  cathode.  The  reaction  is  brought  about  in 
the  same  manner  as  the  orientation  to  light.  When  the  current  is 
made  or  reversed  the  animal  turns  toward  the  dorsal  side  and  continues 
the  turning  until  the  anterior  end  is  directed  toward  the  cathode. 

Thus  the  direction  of  turning  is  throughout  dependent  on  an  internal 
factor,  not  primarily  on  the  way  in  which  the  stimulus  impinges  on 
the  organism.  These  reactions  of  the  Rotifera  are  thus  inconsistent 
with  a  theory  of  tropisms  which  regards  orientation  as  a  primary 
feature  of  the  reactions,  and  which  holds  that  the  action  of  the  stimu- 
lating agent  is  a  direct  one  on  the  motor  organs  of  that  part  of  the 
body  on  which  it  impinges.  The  reactions  of  the  Rotifera,  so  far  as 
described  in  the  preceding  pages,  are  brought  about,  like  those  of  the 
infusoria,  by  what  may  be  called  the  method  of  ''trial  and  error." 
The  reaction  to  any  stimulus  is  of  such  a  nature  as  to  head  the  organism 
successively  in  many  different  directions.  That  direction  is  followed  in 
which  there  is  no  stimulus  to  induce  further  turning. 


FOURTH    PAPER. 


THE  THEORY  OF  TROPISMS, 


CONTENTS. 


PAGE. 


To  what  Extent  does  the  Theory  of  Tropisms  throw  Light  on  the  Behavior 

of  Lower  Organisms  ?..........  91 

Essential  Points  in  the  Theory  of  Tropisms,       ......  92 

Reactions  to  Mechanical  Stimuli,       ........  94 

Reactions  to  Chemicals,     .          .          ........  96 

Reactions  to  Heat  and  Cold,       .........  98 

Reactions  to  Changes  in  Osmotic  Pressure,         ......  98 

Reactions  to  Light,    ...........  98 

Reactions  to  Gravity,          ..........  100 

Reactions  to  Electricity,     ..........  100 

R^sum^  and  Discussion,     .         .         .         .         .         .         .         .         .  .103 

Summary, 106 

90 


THE  THEORY  OF  TROPISMS. 


TO  WHAT  EXTENT  DOES  THE  THEORY  OF  TROPISMS  THROW 
LIGHT  ON  THE  BEHAVIOR  OF  LOWER  ORGANISMS? 

The  writer  has  been  engaged  for  a  number  of  years  in  a  study,  as 
exact  and  detailed  as  possible,  of  the  behavior  and  reactions  of  a  num- 
ber of  lower  organisms.  While  the  results  obtained  have  not,  as  a 
rule,  agreed  with  the  view  that  the  behavior  of  these  organisms  is 
determined  largely  in  accordance  with  the  prevailing  theory  of  tropisms 
or  taxis,  he  has  not  discussed  their  relation  to  this  theory  in  detail. 
This  was  because  of  the  possibility  that  the  reactions  which  he  had 
studied  were  exceptional,  and  that  further  investigation  might  show 
after  all  that  the  behavior  of  the  lower  organisms  is  largely  in  accord- 
ance with  the  tropism  schema. 

At  the  present  time  the  writer  feels  that  the  work  which  he  has 
done,  or  which  has  been  done  by  those  associated  with  him,  is  of  suffi- 
cient extent  to  justify  the  pointing  out  of  certain  general  relations. 
The  reactions  of  ciliate  infusoria,  which  have  long  been  used  as  the 
types  of  illustration  for  the  tropisms,  have  been  examined  in  much 
detail,  and  less  extensive  studies  have  been  made  on  the  Bacteria 
(Jennings  &  Crosby,  1901),  the  Flagellata,  and  the  Rotifera.  The 
reactions  of  a  flatworm  have  been  studied  in  much  detail  (Pearl, 
1903),  and  researches  are  nearly  ready  for  publication,  by  investigators 
associated  with  the  author,  on  the  behavior  of  Hydra  and  of  the  leech, 
and  still  other  studies  are  under  way.  Thorough  studies,  directed  to 
the  observation  of  the  exact  movements  of  organisms  under  stimuli, 
have  recently  been  given  us  by  other  observers  also.  It  seems,  there- 
fore, worth  while  to  bring  out,  in  a  preliminary  way  at  least,  the 
relation  of  the  observations  made  to  the  prevailing  theories  of  animal 
behavior.  In  the  present  paper  this  will  be  limited  to  a  consideration 
of  the  theory  of  tropisms,  since  this  is  the  theory  most  widely  held. 

The  great  apparent  value  of  the  theory  of  tropisms  or  taxis  lies  in 
the  fact  that  it  seems  to  reduce  to  very  simple  factors  a  large  number 
of  the  most  striking  activities  of  organisms,  namely,  those  involved  in 
going  toward  or  away  from  sources  of  stimuli  of  almost  any  character. 
It  is  a  schema,  in  accordance  with  which  almost  any  movements  of  the 
organism  (not  purely  random)  might  be  supposed  to  take  place. 

91 


92  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


ESSENTIAL  POINTS  IN  THE  THEORY  OF  TROPISMS. 

The  two  essential  features  of  the  theory  of  tropisms  are  apparently 
the  following:  (i)  The  movements  of  organisms  toward  certain 
regions  and  their  avoidance  of  others  are  due  to  orientation  ;  i.  e.^  to 
a  certain  position  which  the  organism  is  forced  by  the  external  stimulus 
to  take,  and  which  leads  the  organism  toward  (or  away  from)  the 
source  of  stimulus,  without  any  will  or  desire  of  the  organism,  if  we 
may  so  express  it,  to  approach  or  avoid  this  region.  (2)  The  external 
agent  by  which  the  movement  is  controlled  produces  its  characteristic 
effect  directly  on  that  part  of  the  body  upon  which  it  impinges.  It 
thus  brings  about  direct  changes  in  the  state  of  contraction  of  the 
motor  organs  of  that  part  of  the  body  affected  as  compared  with  the 
remainder  of  the  body,  and  to  these  direct  changes  are  due  the  changes 
shown  in  the  movements  of  the  organism.  This  is  brought  out  clearly 
in  the  quotation  from  Verworn  given  on  page  8.  Loeb  (1900,  p.  7) 
sums  up  the  theory  of  tropisms  as  follows : 

The  explanation  of  them  [the  tropisms]  depends  first  upon  the  specific  irrita- 
bility of  certain  elements  of  the  body  surface,  and,  second,  upon  the  relations 
of  symmetry  of  the  body.  Symmetrical  elements  at  the  surface  of  the  body 
have  the  same  irritability;  unsymmetrical  elements  have  a  diflferent  irritability. 
Those  nearer  the  oral  pole  possess  an  irritability  greater  than  that  of  those 
near  the  aboral  pole.  These  circumstances  force  an  animal  to  orient  itself  toward 
a  source  of  stimulus  in  such  a  way  that  symmetrical  points  on  the  surface  of  the 
body  are  stimulated  equally.  In  this  way  the  animals  are  led  without  will  of 
their  own  either  toward  the  source  of  stimulus  or  away  from  it. 

Holt  &  Lee  (1901)  again  bring  out  our  second  point,  as  applied 
to  reactions  to  light,  with  especial  clearness : 

The  phenomena  that  have  led  to  such  an  assumption  can  be  satisfactorily 
explained  on  the  simpler  theory  that  every  ray  of  light  impinging  on  an  organism 
stimulates  at  the  point  on  ivhicJi  it  falls  *  and  in  proportion  to  its  intensity.  ♦  *  * 
The  light  operates,  naturally,  on  the  part  of  the  animal  which  it  reaches.  The 
intensity  of  the  light  determines  the  sense  of  the  response,  whether  contractile 
or  expansive,  and  the  place  of  the  response,  the  part  of  the  body  stimulated, 
determines  the  ultimate  orientation  of  the  animal."  (Holt  &  Lee,  1901,  pp. 
479-480.) 

The  theory  of  tropisms  as  above  set  forth  depends  upon  the  reflex, 
contractility  of  the  motor  organs  when  affected  by  certain  stimuli.  An 
attempt  has  been  made  to  give  it  a  still  simpler  form  in  a  recent  paper 
by  Ostwald  (1903).  Ostwald  would  omit  even  the  factor  of  reflex 
irritability,  holding  that  the  turning  which  brings  about  orientation  is 
a  mechanical  result  of  differences  in  the  internal  friction  of  the  water  or 


Original  not  italicized. 


THE    THEORY    OF    TROPISMS.  93 

similar  physical  differences.  The  organism  is  considered  to  continue 
to  move  its  motor  organs  in  exactly  the  same  way  after  the  external 
change  (usually  called  a  stimulus)  has  taken  place  ;  the  reason  for  turn- 
ing lies  only  in  the  different  mechanical  effect  produced  when  the  motor 
organs  act  on  a  medium  of  greater  or  less  internal  friction  than  before. 

It  is  difficult  to  conceive  how  anyone  having  any  acquaintance  with 
the  movements  of  organisms  could  propose  such  a  theory  as  that  of 
Ostwald,  and  indeed  this  author  states  (p.  24)  that  his  account  is  purely 
theoretical,  and  that  he  has  not  attempted  to  test  his  theory  by  experi- 
ment. We  need  not,  therefore,  dwell  upon  the  theory,  further  than  to 
point  out  the  fact  that  the  reactions  of  many  of  these  lower  organisms 
have  been  studied  thoroughly,  and  the  reflex  movements  which  they 
perform  when  subjected  to  directive  stimuli  have  been  fully  described, 
and  that  these  movements  are  entirely  incompatible  with  such  a  theory 
as  that  which  Ostwald  sets  forth.*  If  details  are  desired,  it  may  be 
pointed  out  that  all  the  observations  brought  in  the  following  that  are 
inconsistent  with  the  theory  of  tropisms  as  dependent  upon  direct 
stimulation  of  the  motor  organs  are  a  fortiori  inconsistent  with  such 
a  theory  as  that  of  Ostwald. 

We  may,  then,  turn  to  the  theory  of  tropisms  as  set  forth  in  the  above 
quotations  from  Verworn,  Loeb,  and  Holt  &  Lee.  Diagrams  illus- 
trating the  method  of  action  of  a  stimulus,  on  this  theory,  are  given  in 
the  first  of  these  contributions  (Figs,  i  and  2). 

How  far  does  this  theory  go  in  explaining  the  behavior  of  the  lower 
organisms.''  "Tropisms"  has  become  the  keyword  everywhere  in 
animal  behavior  ;  it  is  supposed  to  furnish  a  ready  explanation  of  most 
of  the  puzzles  which  we  here  encounter.     How  far  is  this  justified.'' 

This  question  can  be  answered  only  by  accurate  observation  of  just 
what  organisms  do   under  the  influence  of  stimuli.     The  theory  of 


♦Some  of  the  assumptions  which  Ostwald  makes  as  a  basis  for  his  physical 
analysis  of  the  swimming  of  the  lower  organisms  are  so  extraordinary  as  to 
deserve  mention  as  curiosities.  He  states,  for  example,  that  as  a  rule  the  lower 
swimming  organisms  which  exhibit  the  tropisms  show  active  movement  vertically 
only  upward;  he  thinks  it  probable  that  cases  where  they  have  been  described 
as  swimming  actively  downward  are  errors ;  that  such  downward  movement  is 
really  only  passive  falling.  Yet  everyone  who  has  worked  with  Paramecium  or 
other  Ciliata  must  know  how  far  from  the  facts  is  this  idea.  In  a  vertical  tube 
Paramecia  hasten  as  freely,  and  almost  as  frequently,  downward  as  upward. 
These  infusoria  by  no  means  collect  at  the  top  in  a  vertical  tube  so  regularly  as 
the  literature  on  geotropism  might  lead  one  to  suppose;  Paramecia  of  this  region 
at  least  are  almost  as  likely  to  collect  at  the  bottom  as  at  the  top.  And  there  is 
little  more  difficulty  in  Paramecium  in  distinguishing  an  active  movement  down- 
ward from  a  passive  one  than  there  is  in  man.  From  my  own  observations  I 
know  that  parallel  statements  could  be  made  for  many  other  free-swimming 
organisms,  including  Metazoa  (Rotifera  and  Crustacea),  as  well  as  Protozoa. 


94  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

tropisms  says  that  certain  definite  things  happen  in  the  change  of 
position  undergone  by  organisms  under  the  influence  of  stimuli ;  that 
the  organisms  perform  certain  acts  in  certain  ways.  The  problem  for 
the  investigator  is,  then,  Do  these  things  happen?  Does  the  organism 
perform  these  acts,  in  these  particular  ways?  These  questions  are  not 
metaphysical ;  they  can  be  answered  by  observation. 

We  have  now  before  us  a  considerable  body  of  exact  observations 
which  permit  us  to  answer  these  questions  for  a  certain  number  of 
organisms.  We  will  here  attempt  to  summarize  these  observations  so 
far  as  they  bear  upon  the  essential  points  in  the  theory  of  tropisms.  In 
particular,  we  will  ask,  (i)  Is  the  observed  behavior  brought  about 
through  orientation,  in  the  way  the  theory  of  tropisms  demands?  (2) 
Does  the  evidence  show  that  the  action  of  a  stimulus  is  directly  upon  the 
motor  organs  of  that  part  of  the  body  on  which  the  stimulus  impinges? 

REACTIONS  TO    MECHANICAL  STIMULI. 

The  reactions  to  simple  mechanical  stimuli,  as  when  the  organism 
is  touched  or  struck  by  a  hard  object  over  a  certain  definite  area  of  the 
body,  of  course  do  not  as  a  rule  present  the  conditions  required  for 
the  production  of  a  tropism,  including  a  definite  orientation.  Yet  it  is 
important  to  bring  out  certain  general  relations  shown  in  these  reactions, 
as  they  throw  light  on  the  reactions  to  stimuli  of  a  different  character. 
f  Most  animals  show  in  one  way  or  another  a  tendency  to  avoid  sources 
of  mechanical  shock.  In  the  higher  organisms  the  reaction  usually 
takes  the  form  of  a  turning  away  from  the  side  stimulated.     The  point 

\  which  needs  to  be  brought  out  here  is  that  in  ciliate  infusoria  the  direc- 
tion of  turning  depends,  not  upon  the  part  of  the  body  stimulated,  but 
upon  an  internal  factor.     Stylonychia  turns  to  the  right,  whether  stimu- 

•  lated  on  the  right  side,  on  the  left  side,  on  the  dorsal  surface,  on  the 
anterior  end,  or  by  a  general  unlocalized  mechanical  shock  ;  and  parallel 
statements  can  be  made  for  other  infusoria.  (For  details  see  Jennings, 
1900.)  We  have  proof,  therefore,  that  the  action  of  the  stimulus  is 
on  the  organism  as  a  whole^  not  merely  upon  the  motor  organs  of 

^  that  region  of  the  body  stimulated.  Further,  it  is  clear  that  the 
response  is  a  reaction  of  the  organism  as  a  whole,  not  one  brought 
about  as  an  indirect  result  of  the  fact  that  certain  motor  organs  have 
received  a  stimulus  to  contraction.*  In  these  respects,  therefore,  the 
reactions  to  mechanical  stimuli  are  different  in  character  from  those 
assumed  to  take  place  in  the  tropisms,  and  even  in  these  unicellular 
organisms  the  processes  taking  place  must  be  more  complex  than  the 

♦This  fact  becomes  still  more  striking  when  we  recall  that  the  reaction  takes 
place  in  the  same  way  in  pieces  from  any  part  of  the  body,  from  which  any  given 
motor  organs  may  have  been  removed.     (Details  in  Jennings  &  Jamieson,  1902.) 


THE    THEORY    OF    TROPISMS.  95 

theory  of  tropisms  assumes.  Certainly  a  reaction  of  the  organism  as  a 
unit,  in  response  to  a  localized  stimulus,  is  a  phenomenon  of  a  higher 
and  more  complex  order  than  would  be  a  simple  contraction  or  other 
direct  change  in  the  motor  organs  at  the  point  stimulated. 

In  the  higher  Metazoa  the  reaction  to  a  slight  mechanical  stimulus 
at  one  side  is  usually  a  turning  either  toward  or  away  from  the  source 
of  stimulus.  So  long  as  we  do  not  analyze  the  process  further,  this 
result  might  be  interpreted  either  as  due  to  the  direct  response,  by  con- 
traction, of  the  muscles  primarily  affected  (thus  in  accordance  with  the 
tropism  theory),  or  as  a  response  of  the  organism  as  a  whole,  depend- 
ent, perhaps,  on  an  alteration  in  its  physiological  condition  brought 
about  by  the  stimulus.  The  former  interpretation  is  doubtless  much 
the  simpler.  But  we  find  in  the  unicellular  organisms  that  this  first 
interpretation  is  impossible,  and  that  we  are  forced  to  the  less  simple 
and  definite  conclusion  that  the  organism  reacts  as  a  whole.  Does  it  ^ 
not  then  become  probable  that  in  the  higher  animals  the  very  simple, 
almost  mechanical,  explanation  is  likewise  incorrect ;  that  we  have  in 
them  a  phenomenon  at  least  as  complex  as  that  found  in  the  unicellular 
animals.^  In  other  words,  should  we  conclude  that  the  reactions  in 
the  higher  Metazoa  are  simpler  and  less  unified  than  in  the  Protozoa.?/ 

Fortunately,  however,  we  are  not  forced  to  base  our  conclusions  on 
general  considerations.  These  reactions  have  been  minutely  studied  in 
very  few  of  the  bilateral  Metazoa,  but  Pearl  (1903)  has  given  us  a 
thorough  analysis  of  the  reactions  of  a  flatworm  (Planaria).  This 
cannot  be  taken  up  in  detail  here,  but  we  may  quote  Pearl's  con- 
clusion in  regard  to  the  positive  reaction.  This  consists  in  a  turning 
toward  the  point  stimulated,  on  a  superficial  view  a  very  simple  reac- 
tion, one  especially  well  fitted  for  explanation  on  the  theory  of  direct 
action  of  the  agent  on  the  motor  organs  of  the  region  stimulated.  Pearl 
concludes,  after  exhaustive  study,  that  the  processes  in  the  reaction  are 
as  follows : 

A  light  stimulus,  when  the  organism  is  in  a  certain  definite  tonic  condition, 
sets  off  a  reaction  involving  (i)  an  equal  bilateral  contraction  of  the  circular 
musculature,  producing  the  extension  of  the  body;  (2)  a  contraction  of  the 
longitudinal  musculature  of  the  side  stimulated,  producing  the  turning  toward 
the  stimulus  (this  is  the  definitive  part  of  the  reaction);  and  (3)  contraction  of 
the  dorsal  longitudinal  musculature,  producing  the  raising  of  the  anterior  end. 
In  this  reaction  the  sides  do  not  act  independently,  but  there  is  a  delicately 
balanced  and  finely  coordinated  reaction  of  the  organism  as  a  whole,  depending 
for  its  existence  on  an  entirely  normal  physiological  condition.      (/.  c,  p.  619.) 

Further  studies  carried  on  under  the  direction  of  the  writer,  and 
soon  to  be  published,  will  show  that  in  certain  other  bilateral  Metazoa 
it  is  equally  impossible  to  explain  the  simple  turning  toward  a  stimulus 
as  a  direct  reaction  of  the  motor  organs  of  the  part  stimulated. 


96  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

It  will  be  important  to  keep  in  mind   the  nature  of  the  reactions  to 
mechanical   stimuli,   especially   in   the   infusoria,   in   considering   the 
reactions  which  are  more  usually  classed  among  the  tropisms. 
REACTIONS  TO  CHEMICALS.* 

The  reactions  to  chemicals  have  been  studied  by  the  present  author 
and  those  associated  with  him  in  many  Ciliata,  in  certain  Flagellata, 
in  the  Bacteria,  the  Rotifera,  and  the  flatworm  ;  further  studies,  not 
yet  published,  have  been  made  on  other  organisms.  Now,  in  regard 
to  our  first  question,  as  to  orientation,  the  following  must  be  said  : 
In  no  case  has  the  typical  reaction  been  found  to  take  the  form  of  an 
orientation,  such  as  is  demanded  by  the  theory  of  tropisms.  In  the 
ciliates,  flagellates,  and  rotifers  the  reaction  has  been  found  to  take  the 
form  of  a  "  motor  reflex,"  a  backing  followed  by  a  turning  toward  a 
certain  structurally  defined  side,  without  regard  to  the  direction  from 
which  the  chemical  is  diffusing.  It  is  this  motor  reflex  that  causes  the 
organisms  to  collect  in  the  region  of  certain  chemicals,  and  to  avoid 
others.     (Details  in  Jennings,  "Studies,"  Nos.  I-X.) 

In  the  Bacteria  the  results  of  our  work  (Jennings  &  Crosby,  1901) 
are  in  agreement  with  those  of  Rothert  (1901).  Here,  again,  in  the 
gatherings  in  certain  chemical  solutions,  or  in  the  avoidance  of  others, 
there  is  nothing  resembling  an  orientation  in  the  lines  of  diffusion. 
The  phenomena  are  brought  about  through  a  reaction  of  the  same 
essential  character  as  the  motor  reflex  of  the  infusoria,  but  still  simpler. 
The  essential  point  is  that  the  Bacteria,  when  stimulated  chemically, 
reverse  the  direction  of  movement.     (Details  in  the  papers  just  cited.) 

In  the  flatworm  the  results  of  the  thorough  study  of  the  chemical 
reaction  by  Pearl   (1903)  maybe  given  in  that  author's  own  words: 

Planaria  does  not  orient  itself  to  a  diffusing  chemical  in  such  a  wa_y  that  the 
longitudinal  axis  of  the  body  is  parallel  to  the  lines  of  diffusing  ions.  Its  reac- 
tions to  chemicals  are  motor  reflexes  identical  with  those  to  mechanical  stimuli. 
The  positive  reaction  is  an  orienting  reaction  in  the  sense  that  it  directs  the 
anterior  end  of  the  body  toward  the  source  of  stimulus  with  considerable  pre- 
cision, but  it  does  not  bring  about  an  orientation  of  the  sort  defined  above.  (Pearl 
loc.  cit.^  p.  701.) 

For  details,  the  original  paper  of  the  author  quoted  must  be  consulted. 
It  may  be  added  that  this  positive  reaction,  by  which  the  anterior  end 
is  directed  toward  the  source  of  stimulus,  is  identical  with  that  which 
takes  place  in  response  to  a  single  mechanical  stimulus.  This  is  analyzed 
above  (p.  95). 

Are  there  any  precise  and  detailed  observations  which  support  the 
idea  that  the  reaction  to  chemicals  is  ever  a  typical  tropism.'*     Before 


♦For  a  statement  of  the  theory  of  tropisms  as  applied  to  chemicals,  see  Loeb 
(1897,  p.  442)  and  Garrey  (1900,  pp.  292,  293). 


THE   THEORY   OF   TROPISMS.  97 

the  method  of  reaction  by  a  "  motor  reflex"  had  been  described  the 
reactions  to  chemicals  had  been  referred  in  a  general  way  to  the  tropism 
schema,  but  critical  observations,  which  would  differentiate  between 
the  possibilities,  have  been  lacking.  It  is  necessary  to  use  the  greatest 
caution  in  this  matter,  as  is  shown  by  the  case  of  Chilomonas.  Garrey 
(1900),  although  he  stated  that  ''  a  study  of  the  mechanics  by  which 
the  organism  is  oriented  or  by  which  it  is  prevented  from  moving 
from  the  ring  into  the  stronger  acid  of  the  clear  area,  or  the  weaker 
acid  surrounding  the  ring,  proved  fruitless,"  nevertheless  concluded 
that  the  reaction  in  this  animal  was  a  case  of  typical  tropism.  In  a 
paper  published  in  the  same  number  of  the  same  journal  (Jennings, 
1900,  a),  I  showed  that  when  the  mechanism  of  the  reaction  is  worked 
out,  this  conclusion  does  not  hold,  but  that  the  reaction  takes  place 
through  a  motor  reflex,  similar  to  that  in  the  Ciliata.  In  cases,  there- 
fore, where  the  mechanism  of  the  reaction  (that  is,  the  exact  movements 
which  the  organism  performs)  has  not  been  worked  out,  conclusions  as 
to  the  nature  of  the  reaction  are  of  little  value.  The  only  case  of  which 
I  know  in  which  an  author  acquainted  with  the  method  of  response  by 
a  "  motor  reflex  "  maintains,  on  the  basis  of  observation,  a  reaction  of 
unicellular  organisms  to  chemicals  in  accordance  with  the  theory 
of  chemotropism,  is  the  case  of  Saprolegnia  swarm-spores,  as  described 
by  Rothert  (1901).  In  this  case  we  are  dealing  with  very  minute 
organisms,  and  Rothert  has  made  no  attempt  to  give  an  analysis  of  the 
relation  of  the  direction  of  turning  to  the  differentiations  in  the  body 
of  the  organism,  such  as  we  found  to  be  necessary  above  for  Chilomonas 
before  the  real  nature  of  the  reaction  could  be  determined. 

Thus  it  is  clear  that  cases  of  true  chemotropism,  in  accordance  with 
the  general  tropism  schema,  are  exceedingly  rare,  if  they  exist  at  all. 
In  almost  all  the  lower  organisms  in  which  this  matter  has  been  care- 
fully studied  it  has  been  demonstrated  that  the  reaction  to  chemicals  is 
of  a  different  type  from  that  demanded  by  the  tropism  theory. 

In  the  discussion  so  far  we  have  devoted  attention  particularly  to  the 
question  of  orientation.  When  we  examine  the  second  question  pro- 
posed, as  to  whether  the  stimulus  acts  directly  upon  the  motor  organs 
of  that  part  of  the  body  on  which  it  impinges,  we  find  the  answer 
somewhat  less  clear  than  it  was  in  the  case  of  mechanical  stimuli.  It 
is  true  that  in  the  Infusoria  and  Rotifera  the  direction  of  turning  is,  as 
in  the  case  of  mechanical  stimuli,  always  toward  a  structurally  defined 
side,  without  regard  to  the  direction  from  which  the  chemical  is  diffus- 
ing, so  that  at  first  view  it  seems  beyond  question  that  the  reaction  is 
no^  due  to  the  direct  action  of  the  stimulus  on  the  motor  organs  of  the 
region  on  which  it  impinges.  While  this  conclusion  is  highly  probable, 
the  observed  facts  do  not  demonstrate  it  for  chemical  stimuli  as  they 


98  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

do  for  mechanical  stimuli.  This^  is  owing  to  the  fact  that  the  organism 
determines  for  itself  the  region  in  which  it  shall  be  stimulated  by  a 
chemical  in  solution,  as  well  as  the  side  toward  which  it  shall  turn. 
Now,  it  appears  that  the  side  on  which,  by  its  own  activities,  it  is,  as  a 
rule,  first  stimulated  by  a  chemical,  is  (usually,  at  least)  opposite  that 
toward  which  it  turns.  (For  details,  see  Jennings,  1902,  a.)  It  could  be 
contended,  therefore,  that  the  direction  of  turning,  in  the  case  of  chemi- 
cal stimuli,  is  a  result  of  the  direct  action  of  the  stimulating  agent  on 
the  side  stimulated.  Such  a  contention  would  have  little  general 
significance,  however,  in  view  of  the  fact  that  the  same  reaction  occurs 
as  a  response  to  various  other  stimuli,  where  this  explanation  is  quite 
impossible. 

In  certain  higher  organisms,  researches  which  were  made  under  the 
direction  of  the  writer  and  are  soon  to  appear  will  show  (i)  that  chemi- 
cal stimuli  may  produce  local  contractions  in  the  part  of  the  body  with 
which  the  chemical  comes  in  contact ;  (2)  that  these  local  contractions 
have  little  to  do  with  the  characteristic  behavior  of  the  animals  when 
subjected  to  chemicals. 

REACTIONS  TO  HEAT  AND  COLD. 

Reactions  to  heat  and  cold  have  been  fully  discussed  in  the  first  of 
these  contributions.  It  is  only  necessary,  therefore,  to  point  out  that 
the  results  are  in  almost  every  detail  parallel  with  those  for  reactions 
to  chemicals,  and  in  the  same  way  and  to  the  same  degree  inconsistent 
with  the  theory  of  tropisms.  In  organisms  higher  than  the  Infusoria 
and  Rotifera,  the  reactions  to  heat  and  cold  have  been  very  little  studied 
from  the  present  point  of  view. 

REACTIONS  TO  CHANGES  IN  OSMOTIC  PRESSURE.* 

In  the  ciliate  infusoria  the  reactions  to  differences  in  osmotic  pressure 
are  identical  with  those  to  chemicals,  save  that  the  organisms  are  much 
less  sensitive  to  osmotic  changes.  (Details  in  Jennings,  1897  and  1899.) 
The  bearing  of  these  reactions  on  the  theory  of  tropisms  is,  therefore, 
the  same  as  was  brought  out  above  in  the  discussion  of  the  reactions  to 
chemicals. 

REACTIONS  TO  LIGHT. 

The  phenomena  shown  in  the  reactions  of  organisms  to  light  have  per- 
haps formed  the  chief  basis  for  the  theory  of  tropisms.  There  is  usually 
a  definite  orientation  shown  by  the  organisms  ;  they  move  with  the  axis 
of  the  body  parallel  with  the  light  rays  either  to  or  from  the  source  of 
light.  The  existence  of  such  orientation  forms  the  basis  of  the  theory 
of  tropisms,  and  has  been  considered  sufficient  in  itself  as  a  proof  of  the 


*  "TonoUxis,"  Massart;  "  Osmotaxis,"  Rothert. 


THE    THEORY    OF   TROPISMS.  99 

theory.  Yet  the  theory  makes  certain  definite  statements  as  to  the  cause 
of  the  orientation  and  the  way  in  which  it  is  brought  about.  These 
statements  are  open  to  observation  and  experiment.  In  most  bilateral 
animals  it  is  indeed  difficult  to  really  test  the  theory.  This  is  because 
these  animals  may  turn  directly  toward  either  side  under  the  influence 
of  light,  and  it  is  difficult  to  tell  whether  this  turning  is  due  to  the  direct 
action  of  the  light  on  the  motor  organs  or  to  a  reaction  of  the  organisms 
as  a  whole  induced  by  some  change  in  physiological  condition  brought 
about  by  the  light.  But  in  the  ciliate  infusoria  we  find  a  set  of  organisms 
so  constituted  as  to  permit  us  to  bring  the  theory  to  a  direct  test.  These 
organisms  are  unsymmetrical,  and,  as  we  have  seen,  the  usual  reaction 
is  by  a  motor  reflex  involving  a  turning  toward  a  structurally  defined 
side.  We  can,  therefore,  arrange  our  experiments  in  such  a  way  that 
the  turning  demanded  by  the  theory  of  tropisms  shall  be  the  opposite 
of  that  usually  produced  in  the  reaction  of  the  organism  as  a  whole,  and 
observe  the  results. 

This  is  what  was  done  with  Stentor  cceruleus^  as  described  in  the 
second  of  these  contributions.  The  result,  as  we  have  seen,  is  that  the 
organism  turns  toward  a  structurally  defined  side,  without  regard  to 
what  is  demanded  by  the  theory  of  tropisms.  The  same  result  was 
obtained  with  a  number  of  flagellates  and  with  a  bilateral  Metazoan — 
the  rotifer  Anurcea  cochlearis. 

Thus,  in  these  cases,  it  is  impossible  to  interpret  the  reactions  as  due 
to  the  direct  action  of  the  light  on  the  motor  organs  of  the  side  on 
which  the  light  impinges.  The  response  is  as  clearly  a  reaction  of  the 
organism  as  a  whole  as  is  the  reaction  to  mechanical  stimuli. 

Now  that  it  has  been  shown  that  orientation  to  light  does  occur  in 
some  cases  in  a  manner  quite  at  variance  with  the  postulates  of  the 
theory  of  tropisms,  and  this  in  organisms  widely  separated  in  structure 
and  classification,  it  can  no  longer  be  held  that  orientation  is,  per  se, 
a  proof  of  the  tropism  theory.  In  other  words,  cases  in  which  orien- 
tation takes  place,  but  in  which  the  manner  in  which  it  is  brought 
about  has  not  been  observed,  can  not  be  assumed  as  cases  of  typical 
tropism,  due  to  the  direct  action  of  the  light  on  the  motor  organs 
of  the  side  affected.  The  reactions  of  flagellates  and  swarm-spores 
to  light,  as  described  by  Strasburger  (1878),  have  long  been  con- 
sidered types  for  the  tropisms.  In  the  second  of  these  contributions 
I  have  shown  that  in  Euglena  and  Cryptomonas  (the  latter  being  one 
of  the  organisms  studied  by  Strasburger)  the  reactions  do  not  take 
place  in  accordance  with  the  tropism  schema.  So  far  as  can  be  judged 
from  Strasburger's  account  the  reactions  of  the  swarm-spores  take  place 
in  essentially  the  same  manner  as  in  the  flagellates.  As  Rothert  (1901) 
has  pointed  out,  there  are  many  details  in  Strasburger's  account  which 


lOO  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

suggest  that  the  explanation  on  the  tropism  schema  is  incorrect.  These 
details  become  intelligible  as  soon  as  we  understand  the  real  method 
of  reaction  as  set  forth  in  the  second  of  these  contributions.  The 
assumption  that  the  reaction  is  a  typical  tropism,  when  only  the  fact  of 
orientation  is  known,  is  as  likely  to  fall  to  the  ground  in  other  cases 
as  in  those  just  mentioned. 

The  reaction  of  bacteria  to  light,  as  shown  by  Bacterium  photo- 
metricum,,  described  by  Engelmann  (1882),  is  a  typical  example  of  a 
reaction  through  a  motor  reflex  not  fitting  the  tropism  schema  at  all. 

To  sum  up,  it  is  clearly  shown  in  certain  cases  that  the  reaction  to 
light  takes  place  in  a  way  that  is  not  consistent  with  the  theory  of 
tropisms,  and  this  is  true  in  some  cases  where  a  pronounced  orienta- 
tion exists.  In  many  cases  of  orientation,  where  it  is  supposed  that 
the  theory  of  tropisms  holds,  this  is  an  assumption,  for  the  observations 
which  would  decide  the  matter  are  lacking. 

REACTIONS  TO  GRAVITY. 

In  no  c^3e  have  the  exact  movements  of  unicellular  organisms  in 
response  to  gravity  been  worked  out  in  the  manner  in  which  this  has  been 
done  for  the  reactions  to  mechanical  stimuli,  chemicals,  heat,  light,  and 
electricity.  We  are,  therefore,  without  the  requisite  data  for  deciding 
whether  these  reactions  agree  with  the  theory  of  tropisms  or  do  not.* 

In  the  higher  organisms  in  which  the  positive  and  negative  reactions 
to  gravity  have  been  observed  (starfish,  holothurians,  flies,  insect  larvae, 
etc.),  the  conditions  are  so  complex  that,  so  far  as  I  am  able  to  see, 
observations  which  are  crucial  for  deciding  as  to  the  mechanism  of  the 
reactions  have  not  been  made  and  perhaps  can  not  be  made. 

REACTIONS  TO  ELECTRICITY. 

As  we  have  seen  in  the  third  section  of  this  paper,  the  reactions  of 
the  rotifer  to  the  continuous  electric  current  do  not  take  place  in 
accordance  with  the  theory  of  tropisms.  Anuraea  shows  a  striking 
orientation  to  the  electric  current,  swimming  directly  to  the  cathode. 
Yet  this  orientation  is  brought  about  in  a  way  that  is  quite  inconsistent 
with  the  tropism  schema.  The  reaction  takes  place  through  a  "  motor 
reflex,"  the  direction  of  turning  is  determined  by  an  internal  factor, 
and  not  by  the  way  in  which  the  current  strikes  the  organism.  The 
reaction  can  only  be  interpreted,  therefore,  as  a  reaction  of  the  organism 
as  a  whole. 


♦In  a  forthcoming  paper  by  the  author,  based  on  work  done  since  the  above 
was  written,  it  will  be  shown  that  the  reactions  of  Paramecium  to  gravity  take 
place  in  the  same  way  as  the  reactions  to  most  other  stimuli,  so  that  they  do  not 
agree  with  the  theory  of  tropisms. 


THE    THEORY    OF   TROPISMS.  lOI 

In  the  reactions  of  the  ciliate  infusoria  to  the  constant  electric  current, 
however,  we  have,  if  nowhere  else,  phenomena  which  show  to  a 
certain  extent  clear-cut  and  undoubted  agreement  with  the  theory  of 
tropisms.  To  this  agreement  with  the  theory  of  tropisms  much  of  the 
widespread  adherence  to  the  tropism  theory  for  reactions  in  general  is 
doubtless  due.  The  reaction  of  infusoria  to  the  electric  current  is  con- 
sidered a  type  for  the  other  reactions  of  organisms. 

Yet,  in  deciding  to  what  extent  the  theory  of  tropisms  helps  us  to 
understand  the  behavior  of  organisms,  certain  striking  facts  in  regard 
to  the  reaction  to  the  electric  current  need  to  be  taken  into  considera- 
tion.    These  are  the  following  : 

(i)  The  reaction  to  the  electric  current  never  takes  place  in  nature. 
As  has  been  repeatedly  pointed  out,  the  electric  reaction  is  a  product 
of  the  laboratory  ;  it  is  a  reaction  which  the  organism  never  gives 
under  normal  conditions.  This  being  true,  it  should  not  be  made  the 
type  for  reactions  in  general  unless  it  can  be  shown  clearly  that  the 
characteristic  features  in  the  effects  of  electricity  on  organisms  are 
present  also  in  the  effects  of  other  agents.  Otherwise  we  may  fall  into 
the  same  error  that  would  exist  if  we  considered  the  contortions  of  a 
person  who  had  grasped  the  electrodes  of  a  powerful  battery  as  a  type 
of  human  behavior  in  general. 

(2)  But  examination  shows  that  the  characteristic  features  of  the 
effect  of  electricity  on  organisms  are  not  present  in  the  case  of  other 
stimuli.  The  electric  current,  as  the  experiments  of  Kiihne  (1864) 
and  Roux  (1891)  have  shown,  polarizes  the  cell.  That  is,  it  divides 
it  into  halves,  differing  in  chemical  reaction.  One  half,  in  the  case 
described  by  Kiihne,  had  apparently  an  acid  reaction,  the  other 
half  an  alkaline  reaction.  In  its  effects  on  free-swimming  organisms 
a  similar  polarity  is  shown.  In  Paramecium,  for  example,  the  cilia 
on  one  half  of  the  body  (where  the  current  is  entering)  are  caused  to 
take  a  certain  position,  while  those  on  the  other  half  (where  the  cur- 
rent is  leaving)  take  the  opposite  position.  No  other  agent  known 
produces  these  polar  effiiCis^  either  chemically  or  in  the  effect  on  the 
motor  organs.  Yet  it  is  to  exactly  these  effects  that  the  orientation 
which  makes  this  reaction  the  type  for  the  tropism  theory  is  due. 

If  other  agents  produce  these  effects  why  are  they  not  known  and 
described  }  There  is  no  great  difficulty  in  observing  these  effects  with 
the  use  of  the  electric  current.^  Just  as  exact  studies  have  been  made 
of  the  reactions  to  other  stimuli ;  yet,  so  far  as  I  am  aware,  no  one 
has  ever  described  any  other  stimulus  as  giving  these  characteristic 
polar  effects.  On  the  contrary,  the  reactions  to  other  stimuli  are  well 
known  not  to  show  these  characteristic  phenomena. 

Since,  therefore,  the  characteristic  phenomena  of  the  reaction  to  the 


I02  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

electric  current  are  not  found  in  the  reactions  to  other  stimuli,  it  seems 
a  perversion  to  make  the  electric  reaction  a  type  for  all  others.  The 
reaction  of  the  infusoria  to  the  electric  current  takes  in  its  characteristic 
features  a  unique  position  among  the  reactions  of  the  organism,  requiring 
special  explanation. 

(3)  In  the  response  of  the  infusoria  to  the  electric  current  there 
appears  also  the  same  type  of  reaction  that  occurs  as  a  response  to  other 
stimuli,  but  obscured  by  the  phenomena  peculiar  to  the  effects  of  the 
current. 

This  fact,  that  the  reaction  to  the  electric  current  is  of  a  dual  char- 
acter, that  the  peculiar  effects  of  the  current  are,  as  it  were,  superposed 
upon  the  usual  method  of  reaction,  is  not  usually  so  clearly  recognized 
as  it  deserves  to  be. 

If  the  constant  current  is  passed  through  a  preparation  containing 
large  numbers  of  some  species  of  the  Hypotricha,  as  Stylon3xhia  or 
Oxytricha,  it  will  be  found  that  the  animals,  practically  without  excep- 
tion, attain  their  orientation  by  turning  toward  the  right  side,  thus 
reacting  as  they  would  to  any  other  stimulus.  Further,  if  after  they 
are  oriented  the  direction  of  the  current  is  reversed,  the  animals  all, 
without  exception,  attain  their  new  orientation  (with  anterior  ends  in 
the  opposite  direction)  by  whirling  toward  their  right  sides.  Thus,  so 
far,  the  reaction  to  the  electric  current  is  identical  with  that  to  other 
stimuli,  and  the  direction  of  turning  is  determined  by  an  internal  factor, 
not  by  the  way  in  which  the  current  strikes  the  organism.  In  these 
respects  the  Hypotricha  agree  with  the  Rotifera. 

But  exact  observation  shows  that  in  the  Hypotricha  there  is  another 
factor  involved  in  the  reaction.  The  characteristic  polarizing  effect  of 
the  current  appears  in  its  action  on  the  motor  organs  that  are  distributed 
over  the  body  surface  ;  those  on  one  half  of  the  body  strike  in  one 
direction,  those  on  the  other  half  in  the  opposite  direction.  Part  of 
these  motor  organs,  therefore,  assist  in  turning  the  organism  in  its  usual 
way  (to  the  right)  ;  part  oppose  this  turning.  The  result  is  that  in 
certain  positions  the  turning  to  the  right  is  opposed  by  the  stroke  of  a 
large  number  of  cilia,  so  that  the  turning  takes  place  more  slowly  than 
usual.  Nevertheless,  in  the  Hypotricha,  the  determining  factor  in  the 
reaction  to  the  electric  current  is  almost  throughout  the  same  as  in 
the  reaction  to  other  stimuli ;  the  direction  of  turning  is  determined  by 
internal  factors,  as  a  reaction  of  the  whole  organism,  not  by  the  direction 
in  which  the  current  strikes  or  passes  through  the  organism.  (Details 
in  the  work  of  Pearl,  1900.) 

If  in  place  of  one  of  the  Hypotricha  we  experiment  with  an  infusorian 
in  which  the  cilia  cover  closely  the  whole  surface  of  the  body,  as  Para- 
mecium, the  peculiar  polarizing  effect  of  the  current  on  the  cilia  of  the 


THE    THEORY    OF    TROPISMS.  IO3 

two  halves  of  the  body  becomes  much  more  powerful,  because  the 
number  of  cilia  aftected  in  this  way  is  much  greater.  The  result  is  that 
it  almost  alone  determines  the  nature  of  the  reaction.  The  direction  of 
turning  is,  therefore,  determined  by  the  way  in  which  the  current  strikes 
the  body,  as  required  by  the  theory  of  tropisms.  But  it  should  be 
recognized  that  this  is  by  no  means  universal  among  the  infusoria ;  in 
doubtless  fully  as  many  cases  the  direction  of  turning  is  determined, 
even  under  the  electric  stimulus,  by  an  internal  factor. 

This  peculiar  dual  character  of  the  reaction  to  the  electric  current — 
one  strong  factor  being  due  to  the  inherent  tendency  of  the  organism 
to  turn  in  a  certain  definite  way,  without  regard  to  the  way  in  which 
the  stimulating  agent  impinges  upon  it — has  been  studied  in  detail  in 
recent  contributions  by  Pearl  (1900),  Putter  (1900),  and  Wallengren 
(1902  and  1903).  We  may  perhaps  compare  it,  without  indicating  any 
similarity  in  details,  to  the  behavior  of  a  person  who  has  taken  hold  of 
the  electrodes  from  a  powerful  induction  coil.  He  attempts  in  various 
ways  to  free  himself  from  the  electrodes.  This  may  be  compared  with 
the  attempt  of  the  infusorian  to  perform  its  usual  reaction  to  strong 
stimuli.  He  also  undergoes  involuntary  contortions,  due  to  the  action 
of  the  electricity  on  his  muscles  ;  these  may  be  compared  with  the  pecu- 
liar effect  of  the  electric  current  on  the  cilia  of  the  infusoria,  causing 
them  to  strike  in  opposite  directions  on  the  two  halves  of  the  body. 

Putting  all  together,  we  are  not  justified  in  taking  the  reaction  of  the 
infusoria  to  the  electric  current  as  a  general  type  for  the  reactions  of 
the  lower  organisms,  because  in  its  characteristic  features  it  differs 
from  all  the  other  known  reactions.  Yet  it  is  exactly  these  unique 
features  that  bring  it  into  (partial)  agreement  with  the  tropism  schema. 

RESUME  AND  DISCUSSION. 

We  have  thus  passed  in  review  the  reactions  of  a  large  number  of 
lower  organisms  to  the  commoner  stimuli,  so  far  as  they  are  known 
from  exact  observations.  We  have  found  that  as  a  rule  they  do  not  fit 
into  the  tropism  schema.  In  the  reactions  to  mechanical  stimuli,  to 
heat  and  cold,  to  chemicals,  to  changes  in  osmotic  pressure,  orientation 
is  not  a  primary  or  striking  factor  of  the  reaction  ;  when  a  common 
orientation  of  a  large  number  of  organisms  occurs,  it  is  a  secondary 
result,  due  to  the  fact  that  the  organisms  are  prevented  from  swimming 
in  any  other  direction.  In  the  reaction  to  light  orientation  is  a  strik- 
ing feature ;  but  the  orientation,  in  certain  precisely  investigated  cases 
at  least,  is  brought  about  in  a  manner  which  is  inconsistent  with  the 
tropism  schema.  In  the  reaction  to  gravity  the  precise  reaction  method 
has  not  been  worked  out.  Only  in  the  reaction  to  the  constant  electric 
current  do  we  have  in  some  organisms  a  partial  agreement  in  principle 


104  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

with  the  requirements  of  the  tropism  theory,  and  this  agreement  is  due 
to  an  effect  on  the  organism  in  the  production  of  which  the  electric 
stimulus  is  unique,  so  far  as  known.  In  none  of  the  reactions  which 
have  been  thoroughly  worked  out,  except  partially  in  the  reaction  to 
the  electric  current,  are  the  phenomena  to  be  explained  on  the  view 
that  the  result  is  due  to  the  direct  action  of  the  stimulating  agent  on  the 
motor  organs  of  the  part  of  the  body  on  which  it  impinges.  In  the 
reactions  to  mechanical  stimuli  and  to  light,  and  in  the  reactions  to 
the  electric  current  in  some  animals,  this  view  is  absolutely  disproved. 
The  direction  in  which  the  organism  turns  is,  in  all  the  well  known 
reactions  of  unicellular  organisms  and  rotifers  (except  in  a  portion  of 
the  reactions  to  the  electric  current) ,  determined  by  an  internal  factor, 
and  predictable  from  the  structure  of  the  organism  without  any  know- 
ledge of  the  direction  from  which  the  stimulating  agent  is  to  come. 

We  should  perhaps  consider  here  a  modification  of  the  original  form 
of  the  tropism  theory  that  has  been  proposed  by  some  authors.  This 
is  in  regard  to  the  assumption  that  the  stimulating  agent  acts  directly 
on  the  motor  organs  upon  which  it  impinges.  For  this  it  is  sometimes 
proposed  to  substitute  the  view  that  the  action  of  the  stimulating  agent 
is  directly  on  the  sense  organs  of  the  side  on  which  the  stimulus  im- 
pinges, and  only  indirectly  on  the  motor  organs  through  their  nervous 
connection  with  the  sense  organs.  When  thus  modified  the  theory,  of 
course,  loses  its  simplicity  and  its  direct  explaining  power,  which  made 
it  so  attractive.  In  order  to  retain  any  of  its  value  for  explaining  the 
movements  of  organisms,  it  would  have  to  hold  at  least  that  the  connec- 
tions between  the  sense  organs  and  motor  organs  are  of  a  perfectly 
definite  character,  so  that  when  a  certain  sense  organ  is  stimulated  a 
certain  motor  organ  moves  in  a  certain  way.  When  we  find,  as  we 
do  in  the  flatworm  (see  the  following  paper),  that  to  the  same  stimulus 
on  the  same  part  of  the  body,  under  the  same  external  conditions,  the 
animal  sometimes  reacts  in  one  way,  sometimes  in  another,  the  tropism 
theory,  of  course,  fails  to  supply  a  determining  factor  for  the  behavior. 

But  can  we  explain  the  reaction  methods  of  the  infusoria  and  other 
animals  which,  as  set  forth  above,  are  inconsistent  with  the  tropism 
theory  in  its  original  form,  on  the  basis  of  the  modification  of  this 
theory,  set  forth  in  the  last  paragraph.?  While  in  the  infusoria  the 
assumption  of  nervous  connections,  etc.,  is  inadmissible,  we  may 
waive  that  objection  and  answer  the  question  proposed  from  an  analysis 
of  the  observed  phenomena.  In  Stentor  or  in  Stylonychia,  for  example, 
we  find  that  the  usual  reaction  to  all  classes  of  stimuli  is  by  backing, 
then  turning  toward  the  aboral  side  ;  in  some  of  the  rotifers  by  turning 
toward  the  aboral  (dorsal)  side.  To  simplify  matters,  we  may  take 
into  consideration  only  the  turning  toward  the  aboral  side.     This  turn- 


THE    THEORY    OF   TROPISMS.  IO5 

ing  is  due  to  a  certain  method  of  movement  of  certain  motor  organs. 
In  the  rotifers  it  is  the  coronal  cilia  which  accomplish  the  turning, 
while  in  the  infusoria  we  know  that  the  adoral  cilia  are  concerned  in 
the  movement.  We  may  take  the  coronal  or  adoral  cilia,  then,  as  rep- 
resentative of  the  organs  active  in  the  turning.  For  convenience  we 
may  designate  these  active  organs  simply  as  x. 

Now,  when  the  animal  is  stimulated  on  the  right  side,  we  find  that"*" 
the  motor  organs  x  move  in  a  definite  way.  On  the  tropism  theory  we  j 
would  conclude,  therefore,  that  the  portion  of  the  right  side  stimulated 
has  nervous  connection  with  the  organs  x.  But  we  find  also  that  when 
stimulated  on  the  left  side,  the  oral  side,  or  the  aboral  side,  the  organs  ^ 
X  move  in  exactly  the  same  manner.  In  other  words,  we  find  that  it 
does  not  depend  on  the  side  stimulated  what  organs  respond,  as  re- 
quired by  the  tropism  theory.  This  theory,  then,  in  its  modified  form, 
is  of  no  more  service  for  these  cases  than  in  its  original  form.  The 
responses  in  the  animals  which  we  have  considered  must,  therefore, 
be  conceived  as  reactions  of  the  organism  as  a  whole,  and  due  to  some 
physiological  change  produced  by  the  stimulus,  not  as  the  result  of 
direct  changes  in  certain  motor  organs  when  they  or  the  parts  with 
which  they  are  most  closely  connected  are  locally  aflfected  by  a  stimu- 
lating agent.  The  facts  show  that  the  parts  act  in  the  service  of  the 
whole,  not  that  the  action  of  the  whole  is  due  to  the  more  or  less  inde- 
pendent irritability  and  activity  of  the  parts. 

Thus  the  facts  brought  out  show  that  the  theory  of  tropisms  is  not 
of  great  service  in  helping  us  to  understand  the  behavior  of  these  lower 
organisms.  On  the  contrary,  the  reactions  of  these  organisms  seem 
as  a  rule  thoroughly  inconsistent  in  principle  with  the  fundamental 
assumptions  of  the  theory. 

The  facts  brought  out  above  are  based  on  a  study  of  what  is,  of  course, 
a  comparatively  small  number  of  organisms.  They  rest  chiefly  on  an 
extensive  study  of  the  ciliate  infusoria,  with  less  thorough  examination 
of  bacteria,  flagellata,  rotifers,  and  a  few  higher  organisms.  Doubtless 
in  organisms  which  are  made  up  of  many  parts  which  are  less  firmly 
bound  together  into  a  unified  body  than  in  those  considered,  we  may 
find  greater  independence  of  action  in  the  parts.  This  seems  to  be  the 
case,  for  example,  in  the  sea  urchin,  with  its  numerous  independently 
acting  spines,  pedicellariae,  tube  feet,  etc.  In  this  animal  Von  Uexktill 
(1900,  1900,  a)  concludes  from  his  extensive  study  of  the  reactions  that 
many  features  in  the  behavior  which  seem  at  first  view  to  be  activities 
of  the  animal  as  an  individual  are  really  due  to  the  independent  reac- 
tions of  the  parts,  so  that  he  can  say  that  while  in  walking,  in  the  case 
of  the  dog,  "  the  animal  moves  its  legs  ;  in  the  sea  urchin  the  legs  move 
the  animal."     This  method  of  behavior  has  a  general  agreement  with 


I06  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

what  is  demanded  by  the  tropism  schema,  though  when  we  come  to 
details  of  the  behavior  of  the  organs  themselves,  this  theory  seems 
unsatisfactory,  even  in  the  sea  urchin. 

Such  organisms  as  the  sea  urchin,  composed  anatomically  and  physio- 
logically of  many  parts,  each  acting  almost  as  an  independent  animal, 
are  certainly  less  common  than  more  unified  animals,  such  as  we  find 
in  the  Infusoria,  the  Rotifera,  the  flatworms,  etc.  For  this  reason, 
therefore,  it  has  seemed  worth  while  to  sum  up  the  real  relations  of  the 
behavior  of  these  organisms  to  the  tropism  theory.  The  unicellular 
animals  are  precisely  those  on  which  the  prevailing  theories  of  tropisms 
or  taxis  have  by  many  writers*  been  chiefly  based.  With  the  demon- 
stration that  the  behavior  of  these  organisms  (as  well  as  of  many  higher 
ones),  is  for  the  greater  part  inconsistent  with  the  tropism  theory,  per- 
haps a  large  portion  of  the  foundation  for  its  acceptance  as  a  general 
formula  for  the  chief  features  in  the  behavior  of  lower  animals  is  cut 
from  beneath  it. 

In  the  following  paper,  on  the  part  played  in  behavior  by  physio- 
logical conditions  of  the  organism,  we  shall  find  other,  and,  as  it  seems 
to  me,  still  more  cogent,  reasons  for  holding  the  tropism  theory  inade- 
quate to  account  for  the  determining  factors  in  the  behavior  of  most 
lower  organisms. 

SUMMARY. 

The  foregoing  paper  consists  of  a  review  of  the  behavior  of  Ciliata, 
Flagellata,  Bacteria ;  of  Rotatoria  and  certain  other  Metazoa,  so  far 
as  known  from  exact  observation  of  their  actions  when  stimulated, 
with  a  view  to  determining  how  far  the  prevailing  theory  of  tropisms 
aids  us  in  understanding  the  behavior  of  lower  organisms. 

The  following  are  considered  the  essential  points  in  the  prevailing 
theory  of  tropisms  :  (i)  That  orientation  is  the  primary  factor  in  deter- 
mining the  movements  of  organisms  into  or  out  of  certain  regions,  or 
their  collection  in  or  avoidance  of  certain  regions ;  (2)  that  the  action 
of  the  stimulus  is  directly  upon  the  motor  organs  of  that  part  of  the 
organism  upon  which  the  stimulus  impinges,  thus  giving  rise  to  changes 
in  the  state  of  contraction,  which  produce  orientation. 

The  reactions  of  the  organisms  above  named  are  then  reviewed  to 
determine  in  how  far  there  is  agreement  with  these  essential  points  in 
the  theory  of  tropisms.     The  following  are  pointed  out: 

The  reactions  to  mechanical  stimuli,  to  chemicals,  to  heat  and  cold, 
and  to  variations  in  osmotic  pressure  have  been  described  in  detail,  and 
it  is  found  that  orientation  is  not  a  primary  nor  a  striking  factor  in 
them.     The  response  in  all  these,  cases  is  produced  through  a  ''  motor 


This,  however,  is  not  true  of  Loeb. 


THE    THEORY    OF    TROPISMS.  I07 

reaction"  consisting  usually  of  a  movement  backward,  followed  by  a 
turning  toward  a  structurally  defined  side.  The  direction  of  turning  is 
thus  determined  by  internal  factors. 

In  the  reaction  to  light  orientation  is  a  striking  factor,  but  the  orienta- 
tion is  not  primary,  being  due  to  the  production  of  the  same  "  motor 
reaction"  described  in  the  last  paragraph.  The  method  of  orientation 
is  incompatible  with  the  idea  that  orientation  is  due  to  the  direct  action 
of  the  stimulus  upon  the  motor  organs  of  the  part  of  the  body  on  which 
the  light  impinges,  for  orientation  occurs  by  turning  always  toward  a 
certain  structurally  defined  side,  without  regard  to  the  part  of  the  body 
struck  by  the  light.  The  turning  may,  therefore,  be  toward  or  away 
from  the  source  of  light,  or  in  any  intermediate  direction.  In  any  case 
it  is  continued  or  repeated  until  the  anterior  end  is  directed  away  from 
the  source  of  light,  when  it  ceases. 

The  exact  method  of  reaction  to  gravity  has  not  been  worked  out  by 
direct  observation. 

In  the  reaction  to  the  electric  current  the  reaction  method  of  the 
rotifer  is  by  a  "  motor  reflex,"  and  is  hence  inconsistent  with  the  tro- 
pism  schema.  In  the  Infusoria  there  is  a  partial  (but  only  partial) 
agreement  with  the  requirements  of  the  tropism  theory.  But  this 
partial  agreement  with  the  theory  is  due  to  certain  peculiar  effects  of 
the  electric  current  which  are  not  known  to  be  produced  by  any  other 
stimulus.  Hence  the  reaction  to  the  electric  current,  far  from  being  a 
type  for  reactions  in  general,  is  a  unique  phenomenon,  demanding 
special  explanation. 

The  general  conclusion  is  drawn  that  the  theory  of  tropisms  does 
not  go  far  in  helping  us  to  understand  the  behavior  of  the  lower  organ- 
isms ;  on  the  contrary  their  reactions,  when  accurately  studied,  are,  as 
a  rule,  inconsistent  with  its  fundamental  assumptions.  The  responses 
to  stimuli  are  usually  reactions  of  the  organisms  as  wholes,  brought 
about  by  some  physiological  change  produced  by  the  stimulus ;  they 
can  not,  on  account  of  the  way  in  which  they  take  place,  be  interpreted 
as  due  to  the  direct  effect  of  stimuli  on  the  motor  organs  acting  more 
or  less  independently.  The  organism  reacts  as  a  unit,  not  as  the  sum 
of  a  number  of  independently  reacting  organs. 


FIFTH   PAPER. 


PHYSIOLOGICAL  STATES  AS  DETERMINING 

FACTORS  IN  THE  BEHAVIOR  OF 

LOWER  ORGANISMS. 


109 


CONTENTS. 


PAGB. 

Nature  and  Evidences  of  Physiological  States,    .         .         .         .         .         .     Jii 

Physiological  States  in  the  Protozoa  (Stentor  as  a  Type),  .         .         .112 

Physiological  States  in  the  Lower  Metazoa  (the  Flatworm  as  a  Type),  .  115 
Changes  in  the  Sense  of  "Tropisms"  and  other  Reactions,  .  .  •  "7 
Changes  in  the  Sense  of  Reactions  with  Changes  in  the  Intensity  of  the 

Stimulus,     .         .         .         .         .         .         .         .         .         .         .         .118 

Interference  of  Stimuli,      .         .         .         .         .         .         .         .         .         .119 

Spontaneous  Movements,  .         .         .         .         .         .         .         .         .120 

Methods  of  Causing  Changes  in  Physiological  States,        ....     120 

Nature  of  Reactions  to  Stimuli,  ........     i2i 

Physiological  States  in  the  Behavior  of  Higher  Animals  as  compared  with 

those  in  Lower  Organisms,  ........     124 

Summary,  .         .         .         .         .         .         .         .         .         .         .         .126 

no 


PHYSIOLOGICAL  STATES  AS  DETERMINING 
FACTORS  IN  THE  BEHAVIOR  OF  LOWER 
ORGANISMS. 


NATURE  AND  EVIDENCES  OF  PHYSIOLOGICAL  STATES. 

In  studying  the  behavior  of  the  lower  organisms  the  units  of  obser- 
vation, the  factors  to  which  especial  attention  has  been  paid  have  been 
usually  the  tropisnis  and  reflexes.  These  factors  may  be  considered 
as  determined  mainly  (i)  by  the  action  of  external  agents  on  the 
organism  ;   (2)  by  the  structure  of  the  organism. 

An  examination  of  the  results  of  the  study  of  reactions  in  the  lower 
animals  up  to  the  present  time  shows,  I  believe,  that  we  must  recog- 
nize another  set  of  factors  in  their  behavior,  of  equal  importance  with 
either  of  those  already  named.  This  set  of  factors  may  be  characterized 
by  the  general  term  physiological  states. 

By  physiological  states  we  mean  the  varying  internal  physiological 
conditions  of  the  organism,  as  distinguished  from  permanent  anatomical 
conditions.  Such  different  internal  physiological  conditions  are  not 
directly  perceptible  to  the  observer,  but  can  be  inferred  from  their 
results  in  the  behavior  of  the  animal.  These  results  are  of  so  marked 
a  character  that  the  inference  to  different  physiological  conditions  is 
beyond  question. 

In  the  study  of  tropisms  and  reflexes  a  considerable  number  of 
instances  have  been  brought  to  light  of  changes  in  the  reaction  methods, 
such  as  can  be  attributed  only  to  changed  physiological  conditions. 
Some  of  these  cases  will  later  be  considered  in  detail  in  this  paper. 
Comparatively  few  investigations  on  the  behavior  of  lower  organisms 
have  been  published  in  which  attention  has  been  consciously  directed 
to  these  physiological  states,  and  in  most  of  these  the  matter  has  been 
taken  up  rather  incidentally.  We  may  mention  as  instances  of  papers 
dealing  more  or  less  with  this  aspect  of  the  matter  that  of  Hodge  and 
Aikins  (1895)  on  Vorticella,  those  of  Von  Uexkiill  (1899,  1900,  1900,  a, 
1903)  on  the  sea  urchin  and  on  Sipunculus,  my  own  on  the  behavior 
of  fixed  Infusoria  (Jennings,  1902),  and  that  of  Pearl  (1903)  on  the 
flatworm.  In  the  study  of  higher  organisms  attention  has  of  necessity 
been  largely  directed  to  the  phenomena  determined  by  varying  physio- 
logical states,  as  these  play  a  striking  part  in  the  behavior. 

In  the  present  paper  an  attempt  will  be  made  to  collect  and  analyze 
a  number  of  the  known  cases  showing  the  influence  of  physiological 
states  on  the  behavior  of  the  lower  animals,  pointing  out  some  of  their 
bearings  on  the  theories  of  behavior. 


112  THE   BEHAVIOR    OF   LOWER    ORGANISMS. 


PHYSIOLOGICAL  STATES  IN  THE  PROTOZOA  (STENTOR 
AS  A  TYPE). 

We  will  take  up  first  the  lowest  organisms  in  which  the  matter  has 
been  studied  in  detail,  that  is,  the  unicellular  animals.  These  are  of 
special  interest  in  view  of  their  entire  lack  of  a  nervous  system.  As 
the  best-known  case  we  may  take  the  behavior  of  Stentor.  This  has 
been  described  in  full  in  a  former  paper  by  the  present  author  (Jennings, 
1902,  a) ;  for  details  this  paper  may  be  consulted. 

When  a  quiet,  extended  Stentor  is  stimulated  by  lightly  touching  it 
or  the  support  to  which  it  is  attached  with  a  rod,  it  reacts  by  giving  a 
definite  reflex,  that  is,  by  contracting  into  its  tube. 

After  this  has  taken  place  once  or  twice  we  find  that  the  Stentor  no 
longer  reacts  as  before.  All  the  external  conditions  remain  the  same ; 
the  stimulus  applied  is  the  same.  Nevertheless,  the  Stentor  does  not 
react.  Therefore,  we  must  conclude  that  the  Stentor  itself  has  changed. 
Its  physiological  condition  is  now  different  from  what  it  was  originally. 
What  the  nature  of  the  change  in  its  condition  is  we  do  not  know,  save 
in  the  fact  that  the  Stentor  in  this  second  condition  does  not  react  as 
does  the  Stentor  in  the  first  condition.  For  the  sake  of  convenience 
we  may  number  the  different  physiological  conditions,  in  order  that  we 
may  determine,  if  possible,  how  varied  these  conditions  are.  We  will 
call  the  physiological  condition  of  the  undisturbed  extended  Stentor, 
before  the  stimulation.  No.  i,  or  the  first  condition.  The  condition 
in  which  the  Stentor  no  longer  responds  to  the  slight  stimulus  we  will 
call  No.  2. 

We  may  frequently  distinguish  still  a  third  condition  in  the  behavior 
under  this  simple  stimulus.  At  first  the  Stentor  reacts  by  contraction 
(condition  i).  Then  it  no  longer  reacts  (condition  2).  Later,  or  in 
other  cases,  it  may  react  to  the  stimulus,  but  by  a  different  method 
from  the  first  reaction.  It  now  bends  over  to  one  side  when  touched 
with  the  rod.  As  set  forth  in  my  previous  paper,  "The  impression 
made  on  the  observer  is  very  much  as  if  the  organism  were  at  first 
trying  to  escape  a  danger,  and  later  merely  trying  to  avoid  an  annoy- 
ance." As  conditioning  this  third  method  of  behavior,  when  all  out- 
ward conditions  are  the  same,  we  must  postulate  a  third  physiological 
state  differing  from  the  other  two  ;  this  we  may  call  condition  No.  3. 

We  may  thus  distinguish  at  least  three  different  physiological  states  in 
the  reactions  to  very  weak  stimuli,  where  the  initial  marked  response 
becomes  a  weak  one  or  disappears.  We  may  now  analyze  in  the  same 
way  the  behavior  under  stimuli  of  a  different  character,  when  there  is 
a  series  of  reactions  which  may  be  considered  of  increasing  rather  than 


PHYSIOLOGICAL    STATES    AS    DETERMININCJ    FACTORS.  II3 

of  decreasing  intensity.  Such  a  case  is  that  described  in  my  previous 
paper,  when  water  mixed  with  carmine  particles  is  allowed  to  reach 
the  disk  of  Stentor. 

The  first  physiological  condition  is  again  No.  i— that  of  the  undis- 
turbed extended  Stentor.  In  this  condition  the  organism  does  not 
respond  to  the  stimulus  at  all.  After  the  stimulus  has  continued 
for  some  time,  the  organism  does  respond  by  turning  into  a  new 
position.  We  have,  therefore,  a  new  physiological  condition.  The 
reaction  in  this  case  is  the  same  as  that  given  in  condition  No.  3, 
described  above.  Whether  the  condition  now  existing  is  the  same  as 
in  the  former  case  we  do  not  know ;  as  we  have  no  positive  evidence 
to  the  contrary,  we  will  number  it  3  also. 

Next,  after  several  repetitions  of  this  reaction,  the  organism  responds 
in  a  still  different  manner,  by  momentarily  reversing  the  ciliary  current. 
Since  the  stimulus  and  other  external  conditions  remain  the  same,  the 
organism  itself  must  have  changed.  We  may  call  its  physiological 
condition  at  the  present  time  No.  4. 

Next,  the  animal  contracts  strongly  and  repeatedly.  This  is  clearly 
the  result  of  a  still  different  physiological  condition  which  we  may  call 
No.  5. 

After  thus  contracting  repeatedly  we  find  that  the  organism  remains 
contracted  much  longer  than  it  did  at  first.  It  is  thus  now  in  a  new 
physiological  condition,  which  we  may  designate  as  No.  6. 

Finally,  it  breaks  its  attachment  to  the  bottom  of  the  tube  and  swims 
away  through  the  water.  Probably,  therefore,  we  should  distinguish 
a  seventh  physiological  state,  corresponding  to  this  reaction.  It  is 
possible,  however,  that  the  breaking  of  the  attachment  is  due  to  the 
strong  contractions  which  characterize  condition  No.  6,  so  that  the 
evidence  for  a  seventh  physiological  condition  is  not  unmistakable,  and 
it  may  be  omitted  from  consideration. 

We  are  able  to  distinguish  clearly,  therefore,  in  the  study  of  these 
two  sets  of  reactions,  at  least  six  different  physiological  states.  In  each 
of  these  states  Stentor  is  a  different  organism,  so  far  as  its  reactions  to 
stimuli  are  concerned.  Clearly,  then,  the  external  stimuli  and  the 
permanent  anatomical  configuration  of  the  body  are  by  no  means  the 
deciding  factors  in  the  behavior.  These  factors,  in  the  reaction  series 
last  described,  permit  at  least  five  different  methods  of  behavior. 
Which  of  these  methods  is  actually  realized  depends  not  on  the  quality 
or  intensity  of  the  stimulus,  nor  on  the  anatomical  structure  of  the 
organism,  but  on  its  physiological  condition. 

I  do  not  wish  to  imply  that  I  hold  that  the  six  different  physiological 
states  above  distinguished  are  sharply  defined,  separate  things.  On 
the  contrary,  it  is  much  more  probable  that  the  different  physiological 


114  "^"^    BEHAVIOR    OF    LOWER    ORGANISMS. 

conditions  form  a  continuum.  We  can,  by  taking  sections,  as  it  were, 
at  different  intervals,  distinguish  at  least  six  actually  different  condi- 
tions ;  but  doubtless  there  exists  every  possible  gradation  from  one  to 
another,  so  that  still  other  actually  different  conditions  could  be  distin- 
guished if  we  had  criteria  for  separating  them.  By  careful  analytical 
experiments  the  number  of  different  physiological  conditions  clearly 
recognizable  could  doubtless  be  increased. 

In  other  unicellular  organisms  doubtless  a  condition  of  affairs  may 
be  found  similar  to  that  set  forth  above  for  Stentor.  Hodge  &  Aikins 
(1895)  showed  that  the  reactions  of  Vorticella  vary  with  its  physio- 
logical condition.  In  the  same  paper  (Jennings,  1902,  a)  in  which 
the  behavior  of  Stentor  was  described,  I  have  shown  that  in  various 
other  fixed  infusoria  (Carchesium,  Epistylis,  etc.)  the  behavior  like- 
wise depends  upon  physiological  states  of  the  organism.  In  the 
free-swimming  infusoria  this  has  not  been  shown  to  be  true,  at  least  to 
any  such  extent.  There  may  two  grounds  for  this.  Firstly,  it  is  proba- 
ble that  in  the  free-swimming  infusoria  the  behavior  is  actually  less 
varied  than  in  the  fixed  species.  A  single  motor  reaction  usually 
removes  them  from  the  action  of  the  stimulus  causing  it,  so  that  there 
is  no  reason  for  a  recourse  to  other  methods  of  reaction,  as  occurs  in 
Stentor.  Secondly,  in  the  free-swimming  infusoria  it  is  difficult,  almost 
impossible,  to  observe  continuously  the  reactions  of  a  given  single 
individual.  This  difficulty  could  doubtless  be  met  by  proper  methods 
of  experimentation,  and  if  this  were  done  it  can  hardly  be  doubted  that 
a  dependence  of  the  reactions  on  the  physiological  states  of  the  organism 
would  be  found  here  also.  Indeed,  we  have  indirect  evidence  that  this 
is  true  in  the  case  of  Paramecium,  in  work  already  published.  Thus, 
in  one  of  my  earlier  papers  (1899,  a^  p.  374)  I  called  attention  to  the 
fact  that  Paramecia  from  different  cultures  often  vary  exceedingly  in 
their  reaction  to  a  given  solution  of  a  chemical.  Still  more  pertinent 
to  the  point  under  consideration  is  the  fact,  described  in  the  first  of  my 
studies  (Jennings,  1897) ,  as  well  as  in  the  recent  paper  of  Putter  (1900), 
of  the  great  difference  in  the  reaction  of  Paramecia  and  other  fixed 
infusoria  when  in  contact  with  a  solid,  as  contrasted  with  their  reaction 
when  not  thus  in  contact.  As  this,  however,  may  be  interpreted  as  an 
interference  of  two  stimuli,  a  discussion  of  the  point  is  reserved  until 
later.  A  study  of  individual  specimens  of  some  of  the  larger  Hypo- 
tricha,  such  as  Stylonychia,  from  the  pointof  view  of  changes  in  reaction 
methods  with  changes  in  physiological  condition,  would  doubtless  bring 
forth  interesting  results. 

Even  in  the  lower  unicellular  organisms,  the  Rhizopoda,  similar 
dependence  of  the  method  of  reaction  on  the  physiological  state  of 
the  organism  is  known  to  exist.     Thus  Rhumbler  (1898,  p.  24:)  has 


PHYSIOLOGICAL   STATES    AS    DETERMINING    FACTORS.  II5 

observed  that  Amoeba  verrucosa  may  at  first  begin  to  ingest  an  Alga 
filament,  then  later,  before  the  ingestion  is  complete,  the  filament  may 
be  ejected.  This  involves  a  change  in  the  physiological  condition  of 
the  Amoeba  ;  otherwise  it  would  not  now  reject  a  certain  object  which 
it  before  ingested. 

PHYSIOLOGICAL  STATES  IN  THE  LOWER  METAZOA  (THE 
FLAT  WORM  AS  A  TYPE). 

Passing  now  to  the  Metazoa,  we  find  in  the  flatworm,  Planaria,  as 
described  by  Pearl  (1903),  a  dependence  of  the  reaction  of  the  organism 
on  its  physiological  condition  similar  to  that  which  we  saw  above  for 
Stentor.  The  flatworm  may  be  considered  typical  of  the  lower  bilat- 
eral Metazoa,  so  that  it  will  be  worth  while  to  subject  some  features 
in  its  behavior  to  a  brief  analysis  from  our  present  point  of  view. 

We  may  examine  for  a  simple  typical  case  the  reactions  to  mechani- 
cal stimuli  applied  to  one  side  of  the  anterior  part  of  the  body.  The 
flatworm  is  touched  on  one  side  with  the  tip  of  a  hair  or  of  a  fine  glass 
rod.  The  resulting  response  is  one  of  two  reactions — the  worm  turns 
either  toward  the  point  stimulated  (positive  reaction)  or  away  from  it 
(negative  reaction).  Typically,  the  positive  reaction  is  given  to  a 
weak  stimulus,  while  the  negative  reaction  results  from  a  strong 
stimulus.  The  words  ''  weak"  and  "  strong"  have,  as  we  shall  see, 
only  a  relative  meaning  when  used  in  this  connection. 

When,  now,  we  ask  which  of  these  reactions  shall  be  given  as  a 
response  to  a  certain  stimulus,  we  find  that  this  depends  upon  the 
physiological  condition  of  the  organism.  Pearl  finds  the  reactions 
determined  by  the  following  definitely  marked  physiological  states : 

1.  Individuals  are  frequently  in  what  may  be  called  a  resting  cow- 
dition.  The  tonus  is  lowered  ;  the  animals  are  very  inactive  and  do 
not  respond  readily  to  stimuli.  This  condition  is  compared  by  Pearl 
with  that  of  sleep  in  higher  animals.  When  a  flatworm  in  this  con- 
dition is  given  a  light  stimulus,  such  as  would  in  an  active  specimen 
induce  a  positive  reaction,  it  does  not  respond  at  all.  If  the  strength 
of  the  stimulus  is  increased,  the  animal  finally  responds  with  a  negative 
reaction,  turning  away  from  the  point  stimulated.  We  may  call  this 
the  condition  of  lowered  tonus. 

2.  In  the  more  usual  active  condition  the  flatworm  gives  the  positive 
reaction  to  a  very  light  touch,  a  negative  reaction  to  a  stronger  stimulus. 
We  may  call  this  the  normal  condition. 

3.  After  the  animal  has  been  repeatedly  stimulated  it  seems  to  become 
excited  ;  it  moves  about  rapidly,  and  now  gives  always  the  negative 
reaction  to  any  mechanical  stimulus  to  which  it  reacts  at  all.  It  behaves 
much  as  many  higher  animals  do  under  the  influence  of  fear.  We  may 
call  this  the  excited  condition. 


Il6  THE   BEHAVIOR   OF  LOWER   ORGANISMS. 

4.  After  the  worm  in  the  excited  condition  has  been  stimulated 
repeatedly  on  one  side,  so  that  it  turns  its  head  steadily  in  the  opposite 
direction,  after  a  time  it  suddenly  changes  its  method  of  reaction.  It 
jerks  backward,,  then  turns  the  anterior  end  quickly  through  a  consider- 
able arc,  usually  toward  the  side  from  which  the  stimulus  is  coming, 
so  that  the  head  now  points  in  an  entirely  new  direction.  Since  the 
stimulus  and  other  external  conditions  remain  the  same,  the  organism 
must  have  passed  into  a  new  physiological  condition,  or  it  would  not 
now  react  in  a  different  way.  We  may  call  this  for  convenience  the 
condition  of  over-stimulation. 

5.  Sometimes  individuals  are  found  which  for  a  brief  period  (two  or 
three  hours)  seem  in  a  much  more  active  condition  than  usual.  They 
move  about  rapidly,  but  do  not  conduct  themselves  like  the  excited 
individuals.  As  they  move  they  keep  the  anterior  end  raised  and  wave 
it  continually  from  side  to  side  as  if  searching.  Specimens  in  this  con- 
dition react  to  almost  all  mechanical  stimuli,  whether  weak  or  strong, 
by  the  positive  reaction,  turning  toward  the  point  stimulated.  Experi- 
mentation failed  to  show  that  this  condition  was  due  to  hunger.  We 
may  speak  of  this  fifth  physiological  condition  as  the  state  of  heightened 
activity. 

In  addition  to  the  effect  of  these  five  well-defined  physiological  states 
on  the  method  of  reaction  to  mechanical  stimuli  at  the  anterior  part  of 
the  body.  Pearl  finds  that  other  less  easily  definable  internal  conditions 
affect  the  reactions.  At  times  an  individual  will  give  the  positive  reac- 
tion to  a  stimulus  of  a  certain  strength  a  few  times,  then  cease  to  give 
it.  On  account  of  these  and  other  complications  due  to  varying  internal 
conditions,  Pearl  concludes : 

It  is  almost  an  absolute  necessity  that  one  should  become  familiar,  or  perhaps 
better,  intimate,  with  an  organism,  so  that  he  knows  it  in  something  the  same 
way  that  he  knows  a  person,  before  he  can  get  even  an  approximation  of  the 
truth  regarding  its  behavior. 

We  have  taken  up  above  only  the  physiological  conditions  influ- 
encing the  reactions  to  simple  mechanical  stimuli  in  the  anterior  region 
of  the  body.  We  find  the  condition  of  affairs  even  here  somewhat 
involved.  When  other  more  complex  stimuli  are  taken  into  considera- 
tion the  results  of  the  interplay  of  change  of  physiological  condition 
and  variations  in  the  stimuli  become,  of  course,  much  more  complicated. 

Thus  we  find  in  the  bilateral  metazoan  Planaria,  as  in  the  unsymmet- 
rical  protozoan  Stentor,  that  we  can  by  no  means  predict  the  behavior 
of  the  individual  from  a  knowledge  of  the  anatomical  structure  and  of 
the  strength  of  the  stimulus.  The  anatomical  structure  limits  the  possi- 
bilities of  reaction  to  several  methods,  which  are,  however,  entirely 
different  or  opposite  in  their  effects  on  the  relation  of  the  organism  to 


PHYSIOLOGICAL    STATES    AS    DETERMINING   I^ACTOHS.  II (^ 

the  stimulus.  Just  which  of  these  reactions  shall  be  given  as  a  response 
to  any  particular  stimulus  depends  on  the  physiological  condition  of 
the  organism.  This  physiological  condition  depends  largely,  as  we 
shall  note  later,  on  the  history  of  the  individual.  Thus  no  single  fixed 
schema,  such  as  we  have  in  the  tropism  theory,  can  ever  possibly 
explain  or  define  the  essential  points  in  the  behavior  of  an  animal. 

Stentor  and  Planaria  may  be  taken  as  typical  examples  of  the  higher 
Protozoa  and  of  the  lower  Metazoa,  respectively.  It  is  true  that  we  are 
not  so  well  informed  as  to  changes  in  physiological  condition  in  other 
lower  organisms  as  in  these  two  cases,  but  this  is  unquestionably  due 
merely  to  the  fact  that  investigation  has  not  been  directed  especially  to 
this  point.  There  are,  however,  many  cases  in  the  literature  which 
explicitly  or  implicitly  show  the  importance  of  physiological  conditions 
in  determining  the  behavior  of  lower  organisms.  A  number  of  these 
cases  may  be  brought  together  here. 

CHANGES  IN  THE  SENSE  OF  "  TROPISMS  "  AND  OTHER 
REACTIONS. 

Loeb  (1893)  and  Nagel  (1894)  have  called  attention  to  the  fact  that 
certain  worms  and  mollusks  respond  to  a  shadow  by  suddenly  with- 
drawing into  their  tubes,  but  that  after  the  first  reaction  has  been  thus 
produced  the  worms  may  no  longer  react.  In  this  "  after  effect  of  the 
stimulus  "  (Loeb)  we  have,  of  course,  a  case  of  changed  physiological 
condition. 

Changes  in  the  sense  of  "tropisms"  belong  here.  Groom  &  Loeb 
(1890)  found  that  larvae  of  Balanus  are  at  certain  times  of  the  day 
positively  phototactic ;  at  other  times  negatively  phototactic.  This 
difference,  in  so  far  as  it  is  independent  of  changed  external  conditions, 
is,  of  course,  due  to  differences  in  the  physiological  condition  of  the 
organism.  Loeb  (1893)  found  that  the  larvae  of  the  moth  Porthesia 
are  positively  phototactic  when  hungry  ;  not  so  after  eating.  Here  we 
have  a  well-defined  physiological  condition  determining  the  nature  of 
the  reaction  ;  hunger  is  one  of  the  most  important  conditions  in  many 
of  the  lower  animals.  Sosnowski  (1899)  and  Moore  (1903)  show  that 
the  geotropism  of  Paramecium  changes  from  negative  to  positive  under 
various  conditions.  Towle  (1900)  and  Yerkes  (1900)  have  shown  that 
the  sense  of  the  phototactic  reaction  in  Entomostraca  is  dependent  on 
the  preceding  treatment  of  the  organism,  mere  transference  with  the 
pipette  often  changing  the  sense  of  the  reaction  from  positive  to  nega- 
tive or  vice  versa.  Such  instances  could  doubtless  be  multiplied 
indefinitely.  Each  case  taken  by  itself  seems  perhaps  of  comparatively 
little  significance.  We  may  look  upon  them,  however,  as  indications  of 
an  extensive  dependence  of  behavior  on  physiological  conditions,  such 


Il8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

as  we  found  in  Stentor  and  the  flatworm.  Thorough  investigation  of 
any  of  these  organisms  from  this  point  of  view  would  doubtless  bring 
to  light  a  variety  of  physiological  conditions  on  which  the  reactions 
depend. 

CHANGES  IN  THE  SENSE  OF  REACTIONS  WITH  CHANGES 
IN  THE  INTENSITY  OF  THE  STIMULUS. 

Must  we  not  bring  under  the  same  point  of  view  the  well-known 
phenomenon  of  a  change  in  the  sense  of  the  reaction  with  a  change  in 
the  intensity  of  the  stimulus.?  As  a  simplest  case  of  this  we  may  take  the 
reaction  of  Stentor  to  mechanical  stimuli.  As  shown  in  the  ninth  of 
my  studies  (Jennings,  1902),  Stentor  reacts  to  a  very  weak  mechani- 
cal stimulus  on  one  side  of  the  disk  by  bending  toward  the  source  of 
stimulus;  to  a  stronger  but  otherwise  similar  stimulus  it  responds  by 
contracting  into  the  tube,  or  (later)  by  bending  in  another  direction. 
In  the  same  way  the  flatworm  reacts  positively  to  a  weak  mechanical 
or  chemical  stimulus,  negatively  to  a  stronger  one.  How  can  we  ex- 
plain these  opposite  reactions  to  stimuli  of  the  same  quality,  differing 
only  in  intensity."* 

We  have  here,  it  seems  to  me,  the  same  phenomenon  shown  in  the 
production  of  a  change  in  physiological  condition  by  a  stimulus.  We 
know  that  even  a  single  stimulus  may  produce  a  changed  physiological 
condition,  as  when  after  a  single  stimulus  the  organism  no  longer 
reacts  as  before.  We  know  also  that  the  nature  of  the  physiological 
condition  determines  the  reaction.  In  the  present  case  we  must  con- 
clude that  a  light  stimulus  throws  the  organism  into  a  certain  physio- 
logical condition,  whose  concomitant  reaction  is  turning  toward  the 
point  stimulated.  A  more  intense  stimulus  induces  a  different 
physiological  condition,  whose  concomitant  reaction  is  a  contraction 
into  the  tube  (Stentor),  or  a  turning  in  the  opposite  direction  (flatworm). 
The  action  of  the  stimulus,  as  we  have  seen  in  the  foregoing  paper 
devoted  to  the  theory  of  tropisms,  cannot  in  most  cases  be  directly  on 
the  motor  organs,  so  that  from  this  point  of  view  also  we  are  almost 
forced  to  the  conclusion  that  the  primary  action  of  the  stimulus  is 
to  change  the  physiological  condition  of  the  organism.  In  any  reac- 
tion to  stimulus  we  would  have,  therefore,  the  following  steps :  The 
stimulus  acting  on  the  organism  changes  its  physiological  condition  ; 
this  physiological  condition  induces  a  certain  type  of  reaction.  In 
determining  what  physiological  condition  shall  be  produced,  the  inten- 
sity of  the  stimulus  is  fully  as  important  as  its  quality. 

We  have  a  similar  reversal  of  the  reaction  as  the  intensity  changes 
in  reactions  to  light.  Many  organisms  are  positive  to  weak  light ; 
negative  to  strong  light.      The  cause  of  this  reversal  of  the  reaction  as 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  IIC) 

the  light  grows  stronger  has  given  rise  to  much  discussion  (see 
Hohnes,  1901  and  1903).  We  have  here,  of  course,  a  parallel  case  to 
the  reversal  of  the  reaction  in  Stentor  or  the  flatworni  under  mechani- 
cal stimuli  of  varying  intensity.  In  the  weak  light  we  must  suppose 
the  organism  to  be  thrown  into  a  certain  physiological  condition,  the 
concomitant  of  which  is  a  certain  type  of  reaction.  In  a  more  intense 
light  a  different  physiological  condition  is  induced,  corresponding  to  a 
different  reaction.  The  fact  that  different  intensities  of  stimuli  do 
cause  different  physiological  conditions  and  different  reactions  is,  of 
course,  familiar  to  us,  both  from  experimentation  on  animals  and  from 
our  own  experience ;  in  the  latter  case  we  usually  call  the  distinctive 
reactions  to  very  intense  stimuli  pain  reactions.  In  the  reversal  of  the 
reaction  to  light  as  the  light  becomes  stronger  we  have,  it  seems  to  me, 
merely  an  instance  of  this  general  phenomenon,  not  differing  in  funda- 
mental character  from  other  instances. 

In  most  of  these  cases  we  have,  of  course,  a  further  problem  in  regard 
to  those  features  of  the  reaction  which  concern  direction.  Why  does 
the  weak  stimulus  on  the  left  side  of  Planaria  cause  a  turning  toward 
that  particular  side  ?  Or,  why  does  a  weak  light  from  a  certain  direc- 
tion cause  Volvox  to  swim  in  that  particular  direction  ?  These  problems 
of  direction  are,  of  course,  not  touched  in  the  foregoing  discussion, 
which,  however,  loses  none  of  its  force  because  these  problems  remain. 
They  are  simply  farther  problems.  The  tropism  theory  gave  a  simple, 
direct  answer  to  these  questions ;  but,  as  we  have  already  shown  in 
the  foregoing  paper,  this  answ^er  was,  in  many  cases  at  least,  not  a 
correct  one.  Possibly  some  combination  of  certain  features  of  the 
tropism  theory  with  a  consideration  of  the  facts  of  changes  in  physio- 
logical condition  may  give  us  a  satisfactory  answer  to  the  problems 
of  direction. 

INTERFERENCE  OF  STIMULI. 

Again,  we  have  in  the  interaction  or  interference  of  stimuli  certain 
phenomena  which  seem  to  fall  under  our  present  point  of  view.  First, 
we  have  the  so-called  cases  of  '*  heterogeneous  induction,'*  where  the 
action  of  one  stimulus  reverses  or  modifies  the  reaction  to  another. 
For  example,  many  cases  are  known  in  which  animals  positively  photo- 
tactic  become  negative,  or  vice  versa^  when  the  temperature  is  changed. 
(For  a  collection  of  such  cases  see  Loeb,  1893,  and  Davenport,  1897, 
p.  199.)  In  these  cases  the  physiological  condition  of  the  organism 
seems  altered  by  one  stimulus  (as  heat  or  cold),  in  sucli  a  way  that  it 
no  longer  reacts  to  another  stimulus  (light)  as  it  did  before.  In  the 
ciliate  infusoria,  specimens  which  are  in  contact  with  solids  do  not 
react  at  all  to  many  agents  which  under  other  circumstances  call 
forth  A  marked  reaction.     Putter  (1900)  has  made  a  special  study  of 


I20  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

this  matter,  describing  especially  the  interference  of  contact  with  the 
reaction  to  heat  and  to  electricity.  In  the  second  of  these  contributions 
(p.  32),  we  have  seen  that  attached  Stentors  do  not  react  at  all  to 
light.  Physically  considered,  there  is  no  necessary  opposition  between 
the  action  of  contact  and  the  action  of  the  other  stimuli  named.  We 
must  conclude  then  that  contact  with  solids  so  alters  the  physiological 
condition  of  the  organism  that  it  no  longer  reacts  to  the  other  stimuli. 

SPONTANEOUS  MOVEMENTS. 

Further,  we  find  that  alterations  in  physiological  condition  may  cause 
definite  movements,  which  take  place  without  external  stimulus.  Such 
are  the  movements  which  we  call  spontaneous.  As  an  example  of  this 
we  may  take  the  case  of  Hydra.  If  an  undisturbed  green  Hydra  is 
observed  continuously,  it  is  found  to  contract  and  again  to  extend  with- 
out visible  cause  every  i^  to  2  minutes.  Thus,  it  remains  at  rest  for 
a  period  of,  say,  i^  minutes.  Its  physiological  condition  at  this  time 
we  may  call  X.  At  the  end  of  this  period  it  contracts.  Since  the 
external  conditions  have  not  changed  the  Hydra  itself  must  have 
changed,  otherwise  it  would  continue  at  rest.  The  physiological  condi- 
tion ^passes  into  the  condition  T^  and  the  Hydra  as  a  result  contracts. 
This  contraction  is,  of  course,  exactly  the  reaction  given  as  a  response 
to  most  stimuli  in  Hydra.  In  Vorticella  we  find  similar  spontaneous 
contractions  at  intervals,  essentially  as  in  Hydra.  Cases  of  movements 
in  the  lower  organisms  that  are  inaugurated  by  internal  changes  in 
condition  could,  of  course,  be  multiplied  indefinitely.  For  our  present 
point  of  view  it  is  of  importance  to  recognize  clearly  the  fact  that  a 
change  in  physiological  condition  may,  by  itself,  cause  exactly  the  same 
behavior  that  at  other  times  appears  as  a  response  to  external  stimuli. 

METHODS  OF  CAUSING  CHANGES  IN  PHYSIOLOGICAL 
CONDITION. 

Changes  in  physiological  condition  are  thus  evidently  brought  about 
in  a  number  of  different  ways.  We  may  attemfft  to  summarize  here 
the  diflferent  methods  which  appear  to  exist  in  the  lower  organisms. 

(i)  A  single  simple  stimulus  may  bring  about  a  change  in  physiologi- 
cal condition.  This  is  proved  by  the  fact  that  the  organism  after  it  has 
received  a  single  stimulus  may  react  differently  from  its  previous 
method.  Thus,  Stentor  reacts  to  a  single  touch,  but  after  this  single 
touch  it  may  no  longer  react  when  touched  in  the  same  way  again  ; 
or  it  may  react  in  a  different  manner.  It  is  probable,  further,  that  the 
first  reaction  to  a  single  simple  stimulus  is  to  be  considered  due  to  a 
change  in  physiological  condition  produced  by  this  stimulus. 

(2)  Repetition  of  the  same  stimulus  may  cause  a  change  in  physio- 
logical condition  such  as  is  not  produced  by  a  single  stimulus.     This 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  121 

again  may  be  illustrated  from  the  experiments  on  Stentor,  described 
above  (p.  112). 

(3)  Internal  causes,  not  definable,  may  give  rise  to  changes  in  physio- 
logical condition.  The  result  is  spontaneous  movement  at  intervals, 
as  described  above  for  Vorticella  and  Hydra.  As  many  authors  have 
pointed  out,  rhythmical  soontaneous  movements  may  be  due  to  a  steady, 
non-rhythmical,  internal  change  of  condition. 

(4)  The  movement  or  reaction  performed  by  the  organism  may 
change  the  physiological  condition.  This  is  illustrated  in  one  way  by 
the  fact  that  after  a  single  spontaneous  contraction  in  Vorticella  or 
Hydra,  the  animal  remains  quiet  for  an  interval,  showing  that  the 
original  physiological  condition  was  restored  by  the  movement.  The 
fact  that  the  reaction  performed  by  the  organism  changes  the  physio- 
logical condition  of  the  latter  is,  of  course,  the  basis  of  the  formation  of 
habits  in  higher  organisms ;  in  this  case  the  performance  of  a  reaction 
once  or  repeatedly  throws  the  organism  into  a  condition  where  it  is 
more  likely  to  react  in  the  same  way  again.  This  particular  method 
of  alteration  of  condition  has  perhaps  not  been  clearly  demonstrated 
for  unicellular  organisms,  though  there  is  some  indication  of  it  in  the 
behavior  of  Vorticella,  as  described  by  Hodge  &  Aikins  (1895),  and 
of  Stentor  as  described  by  myself  in  the  ninth  of  my  studies.  Thus, 
Stentor  responds  to  carmine  in  the  water  by  a  series  of  different  reac- 
tions, finally  reaching  the  condition  where  it  reacts  by  contracting  at 
once  into  its  tube.  If  the  stimulus  is  now  repeated  every  time  the 
Stentor  extends,  it  never  gives  its  earlier  method  of  reaction,  but  reacts 
steadily  for  a  long  time  by  contracting  at  each  stimulus.  Is  this  persist- 
ence in  the  contraction  reaction  due  partly  to  the  fact  that  it  has  begun 
on  this  reaction  method,  and  therefore  keeps  it  up,  or  is  it  due  only  to 
the  fact  that  the  stimulus  has  been  repeated  many  times  ?  In  the  former 
case  the  behavior  would  perhaps  fall  under  our  present  point  of  view ; 
in  the  latter  it  would  not.  Cases  among  the  Protozoa  where  the  repeated 
performance  of  a  reaction  clearly  makes  the  further  performance  of  the 
same  reaction  easier  or  more  likely  to  occur,  would  be  of  much  interest. 

NATURE  OF  REACTIONS  TO  STIMULI. 

The  foregoing  considerations  evidently  have  a  definite  bearing  on 
the  problem  of  the  nature  of  reactions  to  stimuli.  They  lead,  as  set 
forth  briefly  on  page  118,  to  the  following  conception  of  the  steps  oc- 
curring in  a  reaction  to  a  stimulus:  (i)  The  stimulus  acting  on  the 
organism  causes  a  change  in  its  physiological  condition ;  (2)  this 
change  in  physiological  condition  gives  rise  to  the  typical  reaction. 

The  evidence  for  this  view  is  found  scattered  throughout  the  fore- 
going discussion  ;  its  main  points  may  be  briefly  summarized  here  as 
follows : 


132  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

(i)  We  have  seen  that  stimuli  do  unquestionably  cause  changes  in 
physiological  condition.  This  is  demonstrated  by  the  fact  that  after  a 
stimulus  has  occurred  and  ceased  to  act,  the  organism  reacts  differently 
to  the  same  or  other  stimuli.    (For  examples  see  pages  112,  117.) 

(2)  We  have  seen  that  the  changes  in  physiological  condition  do  un- 
questionably cause  definite  movements,  of  exactly  the  sort  that  we  are 
accustomed  to  call  reactions  to  stimuli.  (Contraction  of  Hydra  or  Vor- 
ticella,  etc. ;  see  p.  120.) 

These  two  facts  give  a  solid  foundation  for  the  above  view  of 
reactions  to  stimuli,  and,  indeed,  it  seems  to  me,  raise  a  presumption 
that  reactions  to  stimuli  are,  as  a  rule,  brought  about  in  the  way 
described.     Further  evidence  in  favor  of  this  view  is  as  follows  : 

(3)  In  the  paper  which  precedes  the  present  one  we  have  demon- 
strated that,  in  the  Infusoria  and  Rotifera  at  least,  the  action  of  stimuli 
is  not  directly  on  the  motor  organs  of  that  part  of  the  body  on  which 
the  stimulus  impinges.  The  organism  reacts  as  a  whole,  and  in  a  way 
that  is  not  explicable  even  on  the  assumption  of  a  definite  plan  of  ner- 
vous interconnection  between  the  regions  stimulated  and  the  motor 
organs,  an  assumption  that  is,  of  course,  in  any  case  not  allowable  for  the 
Infusoria.  Such  reactions  cannot  be  explained  otherwise  than  as  due 
to  changes  in  the  physiological  condition  of  the  organism  as  a  whole. 
Further,  evidence  was  given  to  show  that  the  reactions  of  higher  organ- 
isms are  in  many  cases  equally  inexplicable  as  a  result  of  direct  action 
of  the  stimulus  on  the  motor  organs. 

Only  in  the  reaction  of  some  organisms  to  the  constant  electric  cur- 
rent did  we  find  such  conditions  fulfilled  as  permit  an  explanation  of  a 
part  of  the  phenomena  on  the  theory  of  the  direct  action  of  the  agent 
on  that  part  of  the  body  on  which  it  impinges,  in  accordance  with  the 
theory  of  tropisms.  Other  features  of  the  reaction  to  this  stimulus  (in 
many  cases  the  determining  ones)  are  only  explicable  on  the  theory 
that  they  are  due  to  the  physiological  state  of  the  organisms  as  a 
whole,  induced  by  the  stimulus  (see  p.  100).  This  shows  that  we  may 
find  at  any  time  these  two  methods  of  action  mixed,  or  perhaps  eithei 
one  separately.  But  the  reaction  to  the  electric  current  is  the  only  one 
out  of  the  reactions  to  a  multitude  of  agents,  that,  in  the  Infusoria,  has 
been  shown  to  have  this  additional  feature — reactions  of  different  parts 
of  the  body  in  opposed  ways.  The  reaction  to  the  electric  current  is 
thus  of  the  very  greatest  interest,  not  because  it  stands  as  type  for 
reactions  in  general,  but  for  exactly  the  opposite  reason,  because  it 
presents  factors  which  are  not  known  to  occur  in  other  reactions. 

(4)  The  view  that  reactions  to  stimuli  take  place  through  the  inter- 
mediation of  changes  in  the  physiological  condition  of  the  organism  as 
a  whole  is  further  reinforced  by  the  fact,  set  forth  above,  that  it  is  only 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  1 23 

on  the  basis  of  such  a  view  that  we  can  understand  the  changes  of 
reaction  which  occur  when  the  same  stimulus  is  repeated ;  by  the  facts 
of  the  interference  of  stimuli,  even  when  their  direct  physical  action  is 
by  no  means  opposed ;  by  the  facts  of  heterogeneous  induction,  and  by 
the  fact  that  organisms  at  different  times  of  the  day  or  at  different  sea- 
sons show  different  methods  of  reaction  to  the  same  stimuli. 

(5)  This  view  is  also  strengthened  by  the  fact  that  it  brings  into 
relation  reactions  to  stimuli  and  spontaneous  movements.  On  this  view 
both  are  due  directly  to  the  same  cause,  to  changes  in  physiological 
condition,  produced  in  one  case  by  internal  causes,  in  the  other  by 
external  causes. 

(6)  This  view  receives  powerful  support,  it  seems  to  me,  in  our 
knowledge  of  what  takes  place  in  the  higher  animals,  including  man. 
This  point  I  shall  attempt  to  develop  farther  on  in  the  present  paper. 

This  view,  that  reactions  to  stimuli  in  the  lower  organisms  are  pro- 
duced in  general  through  changes  in  physiological  condition,  is  not,  of 
course,  set  forward  as  anything  new  or  original.  Many  others  have 
doubtless  taken  this  point  of  view,  and  it  is  implied,  perhaps  not  always 
consciously,  in  many  attempted  explanations  of  animal  behavior. 
The  writer  is  merely  attempting  to  emphasize  that  particular  interpre- 
tation, out  of  many  existing  ones,  towards  which  the  facts  seem  to 
point  strongly.  He  is  convinced  that  the  factor  of  physiological  con- 
dition as  determining  behavior  has  not  Deen  so  fully  and  explicitly 
realized  and  dealt  with  in  work  on  the  lower  organisms  as  the  facts 
demand,  and  that  many  things  that  seem  anomalous  fall  into  their 
proper  places  when  this  factor  is  taken  fully  into  consideration. 

What  is  the  nature  of  physiological  conditions,  or  changes  in  phys- 
iological condition.?  Of  course,  we  are  not  able  to  answer  this  ques- 
tion. One  is  tempted  to  think  of  these  expressions  as  signifying 
something  like  chemical  states  or  changes  in  chemical  states.  But  the 
concept  of  physiological  states  is,  for  higher  animals  at  least,  one  at 
which  we  arrive  by  analysis  of  complex  phenomena  in  behavior,  and 
this  does  not  give  us  any  direct  evidence  as  to  the  real  nature  of  the 
change  in  the  living  substance  (considered  as  matter)  which  takes 
place  when  the  physiological  condition  changes. 

The  concept  ''  physiological  states"  is  a  preliminary  collective  con- 
cept, which  may  later  be  analyzed  into  many.  Such  analysis  is  certain, 
however,  to  be  difficult  and  hypothetical  in  character  in  the  lowest 
organisms.  In  man  we  have,  of  course,  a  basis  for  analysis  in  the  sub- 
jective accompaniments  of  physiological  (here  called  psychological) 
conditions, — in  the  feelings,  emotions,  etc. 


124  THE   BEHAVIOR    OF   LOWER    ORGANISMS. 

PHYSIOLOGICAL    STATES    IN  BEHAVIOR  OF  HIGHER  ANIMALS, 
AS  COMPARED  WITH  THOSE  IN  LOWER  ORGANISMS. 

Realization  of  the  fact  that  the  behavior,  even  in  the  lowest  organisms, 
is  determined  to  a  large  degree  by  physiological  states  must  be  of  great 
service  in  welding  into  one  connected  whole  the  study  of  behavior  in 
all  animals,  from  the  lowest  up  to  man.  The  attempt  to  divorce  the 
study  of  the  behavior  of  man  from  that  of  the  lower  animals,  which 
has  been  evident  in  late  years,  seems  unfortunate  and  unnecessary.  It 
is  true  that  we  are  not  justified  in  reading  the  subjective  states  of  man 
directly  into  the  lower  organisms.  But  we  are  not  confronted  with  the 
alternative  of  doing  this  or  of  separating  the  two  subjects  completely. 
The  behavior  of  man  can  be  studied  from  the  same  objective  standpoint 
which  we  employ  in  investigating  the  behavior  of  animals.  When  this 
is  done,  there  is  no  reason  for  holding  the  results  on  man  aloof  from 
those  obtained  elsewhere ;  if  it  is  proper  to  compare  different  organ- 
isms of  any  kind  from  this  point  of  view,  in  order  to  obtain  general 
results,  as  all  investigators  do,  it  is  certainly  proper  to  draw  man  also 
into  the  circle  of  comparison.  The  fact  that  in  man  we  can  know  also 
the  subjective  accompaniments  of  the  different  physiological  states  and 
reactions  is  by  no  means  a  disadvantage  in  this  comparison  ;  it  is  merely 
an  additional  feature,  of  the  highest  possible  interest.  We  can  even, 
it  seems  to  me,  justifiably  call  attention  to  the  relation  between  the 
subjective  states  as  found  in  man  to  certain  general  phenomena  common 
to  man  and  other  organisms.  It  is  only  when  we  proceed  directly  to 
attribute  to  the  lower  animals  the  subjective  states  which  we  know  only 
in  man  (and,  indeed,  only  in  our  own  individual  mind?)  that  we  pass 
the  boundary  of  scientific  procedure. 

In  the  higher  animals,  and  especially  in  man,  the  essential  features 
in  behavior  depend  very  largely  on  the  history  of  the  individual ;  in 
other  words,  upon  the  present  physiological  condition  of  the  individual, 
as  determined  by  the  stimuli  it  has  received  and  the  reactions  it  has 
performed.  But  in  this  respect  the  higher  animals  do  not  differ  in 
principle,  but  only  in  degree,  from  the  lower  organisms,  as  we  have  seen 
in  our  analysis  of  the  behavior  of  Stentor.  In  this  unicellular  form 
we  were  forced  to  distinguish  at  least  six  different  physiological  condi- 
tions, determining  in  the  same  individual  different  reactions  to  the  same 
stimuli.  In  the  higher  animals,  and  especially  in  man,  we  can  distin- 
guish, as  might  be  expected,  an  immensely  greater  number  of  such 
conditions  which  induce  different  reactions,  but  there  is  no  evident  differ- 
ence in  principle  in  the  two  cases.  Can  we  go  farther  and  make  a  more 
direct  comparison  of  individual  physiological  states  in  the  higher  and 
lower  organisms?  We  find  in  Stentor,  and  again  in  the  flatworm, 
that  after  the  organism  has  been  repeatedly  stimulated  by  an  agent 


PHYSIOLOGICAL   STATES   AS   DETERMINING   FACTORS.  1 25 

which  must  in  the  long  run  be  classed  as  injurious,  it  is  thrown  into  a 
physiological  condition  in  which  its  reactions  become  more  rapid  and 
powerful,  and  of  such  a  nature  as  to  remove  the  organism  from  thfe 
source  of  stimulus.     We  find  that  in  this  state  the  organism  reacts  to  i 
any  stimulus  to  which  it  reacts  at  all  by  a  strong  negative  reaction,  j 
In  higher  animals  we  frequently  find  the  same  condition  of  affairs,  andj 
the  animal  is  then  commonly  said  to  be  frightened.     Finally,  we  often\ 
find  in  man  a  similar  condition,  and  here  we  know  certain  subjective i 
accompaniments  of  the  physiological  condition,  the  most  characteris-^> 
tic  of  which  is  perhaps  the  emotion  of  fear.     In  all  these  cases  the 
objective  manifestations  of  the  physiological  condition  are  of  the  same 
character.     Does  the  fact  that  in  man  we  know  something  additional 
about  the  matter,  the  subjective  accompaniments,  constitute  grounds 
for  denying  the  essential  similarity,  from  a  physiological  standpoint, 
of  this  condition  in  man  and  that  in  the  lower  organisms  ?     It  seems  to 
me  that  it  does  not ;  in  fact,  all  that  is  maintained  in  making  the  com- 
parison is  that  this  condition  causes  similar  objective  phenomena  and 
is  brought  about  by  similar  conditions.    Further  than  this  our  analysis 
and  comparison  cannot  go. 

Another  class  of  physiological  conditions  which  we  can  distinguish  ? 
almost  all  the  way  through  the  animal  series  is  that  produced  character- 
istically by  intense  stimuli,  as  opposed  to  faint  stimuli.  As  a  rule,  any 
stimulus,  even  if  it  is  one  to  which  the  organisms  respond  usually  by  a 
positive  reaction,  produces,  when  it  becomes  very  intense,  reactions 
whose  general  effect  is  to  remove  the  organisms  from  the  source  of 
stimulation  (negative  reactions).*  This  is  true  in  Amoeba,  where  weak 
mechanical  stimuli  cause  spreading  out  and  movement  toward  the 
source  of  stimulus,  while  strong  mechanical  stimuli  cause  it  to  contract 
and  move  away ;  it  is  true  for  Stentor ;  it  is  true  for  the  stimulus  of 
weak  and  strong  light  in  Euglena  and  Volvox  and  many  other 
organisms ;  it  is  true  for  mechanical  and  chemical  stimuli  in  the  flat- 
worm  ;  it  is  true  in  general  for  higher  animals  and  man.  In  all  these 
cases  the  intense  stimulus  evidently  changes  the  physiological  con- 
dition so  that  the  organism  now  reacts  negatively.  In  man  we  know> 
that  this  physiological  condition  is  accompanied  subjectively  by  pain' 
or  at  least  discomfort,  and  even  in  higher  animals  such  reactions  are 
usually  spoken  of  as  pain  reactions.  Objectively  considered,  the 
phenomena  are  analogous  throughout  the  animal  series,   so  that  we 


*  "All  organisms  behave  in  two  great  and  opposite  ways  toward  stimulations  ;^ 
they  approach  them  or  they  recede  from  them.     Creatures  which  move  as  av 
whole  move  toward  some  kinds  of  stimulations,  and  recede  from  others.     Crea-  • 
tures  which  are  fixed  in  their  habitat  expand  toward  certain  stimulations,  and/ 
contract  away  from  others."     Baldwin,  1897,  p.  199. 


126  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

I  may  properly  characterize  the  physiological  condition  which  produces 

j  the  negative  reaction  to  strong  stimuli,  with  Professor  J.  Mark  Bald- 

\  win  (1897,  p.  43)   as  the  ''  physiological  analogue  of  pain."    This,  of 

course,  by  no  means  commits  us  to  the  belief  that  the  organisms  have 

a  sensation  of  pain  ;  concerning  this  we  know  nothing. 

It  thus  seems  to  me  possible  to  trace  some  of  the  physiological  con- 
ditions which  we  know,  from  objective  evidence,  to  exist  in  man  and 
the  higher  animals,  back  to  the  lowest  organisms.  Many  conditions  that 
we  can  clearly  distinguish  in  man  will  doubtless  be  followed  back  to  a 
common  single  condition  in  the  lower  organisms  ;  but  this  is  exactly  what 
we  should  expect.  Differentiation  takes  place  as  we  pass  upward  in 
the  scale,  in  these  matters  as  in  others. 

The  most  interesting  and  important  field  in  which  we  find  the 
behavior  of  higher  organisms  dependent  on  their  previous  history,  and, 
therefore,  on  their  present  condition  as  influenced  by  previous  experi- 
ence, is  in  that  group  of  phenomena  which  we  call  memory,  or  learning 
by  experience.  Memory  has  as  its  basis  the  general  phenomenon  that 
a  stimulus  received  or  a  reaction  performed  leaves  a  trace  on  the 
organism,  or  modifies  its  condition  in  such  a  way  that  it  later  reacts 
differently  to  the  same  stimulus.  This  basis  of  memory  is,  of  course, 
clearly  present  in  Stentor. 

The  analysis  of  the  different  physiological  conditions  found  in  the 
lower  organisms,  the  influences  to  which  they  are  due,  and  the 
reactions  of  these  organisms  as  influenced  by  physiological  conditions 
certainly  forms  a  most  promising  field  for  research,  and  one  as  yet 
almost  untouched. 

SUMMARY. 

The  present  paper  attempts  to  show,  by  an  analysis  of  certain 
phenomena  in  the  behavior  of  lower  organisms,  taking  Stentor  and 
Planaria  as  types,  that  physiological  states  of  the  organism  are  most 
important  determining  factors  in  reactions  and  behavior.  In  these 
organisms,  to  the  same  stimuli,  under  the  same  external  conditions, 
the  same  individuals  react  at  different  times  in  radically  different  ways, 
showing  the  existence  of  different  physiological  states  of  the  organism, 
which  determine  the  nature  of  the  reactions.  In  a  unicellular  organ- 
ism (Stentor)  we  can  distinguish  at  least  six  different  physiological 
states,  in  each  of  which  the  organism  has  a  different  reaction  method, 
and  corresponding  facts  are  brought  out  for  the  flatworm.  Scattering 
observations  taken  from  works  on  tropisms,  etc.,  are  shown  to  indicate 
that  the  same  state  of  affairs  is  found  in  other  lower  organisms. 

The  conditions  producing  these  different  physiological  states  are 
examined  and  their  importance  for  the  theory  of  behavior  in  the  lower 
organisms  is  brought  out.     The  relations  of  these  facts  to  "  interference 


PHYSIOLOGICAL    STATES    AS    DETERMINING   FACTORS.  1 27 

of  stimuli,"  "heterogeneous  induction,"  "spontaneous  movements," 
and  "changes  in  the  sense  of  reactions  with  a  change  of  intensity  in 
the  stimulus,"  are  developed. 

The  view  is  set  forth  that  in  most  of  the  lower  organisms  a  reaction 
to  stimulus  usually  involves  the  following  factors:  (i)  the  stimulus 
changes  the  physiological  state  of  the  organism  as  a  whole ;  (2)  this 
change  in  physiological  state  induces  a  certain  type  of  reaction. 
Evidence  for  this  view  is  summarized. 

Finally,  it  is  pointed  out  that  realization  of  the  importance  of 
physiological  states  as  determining  factors  in  the  behavior  of  the  lower 
organism  is  of  service  in  bringing  the  study  of  these  organisms  into 
relation  with  that  of  higher  animals  and  man.  An  objective  study  of 
the  behavior  of  these  higher  animals  shows  the  prevalence  of  physio- 
logical states  as  determining  factors  in  behavior,  and  in  some  cases,  at 
least,  some  of  these  states  are  closely  analogous  to  what  we  find  even 
in  unicellular  organisms. 


SIXTH    PAPER 


THE  MOVEMENTS  AND  REACTIONS 
OF  AMCEBA. 


139 


CONTENTS. 


Introduction:  Objects  of  the  Investigation, 131 

Description  of  the  Movements  and  Reactions, 132 

The  Movements, 132 

The  Movements  of  Amoeba  as  described  Formation  and  Retraction  of  Pseudopodia  15a 

by  Rhumbler  and  Butschli ;  Agree-  Surface    Currents    in    Formation    of 

ment  with  Currents  in  a  Drop  of  Pseudopodia  in  contact  with  Sub- 


Fluid  Moving  as  a  Result  of  a  Local 

Decrease  in  Surface  Tension 132 

Currents  in  Amoeba  as  studied  from  above; 


stratum 152 

Formation  of  Free  Pseudopodia 153 

Withdrawal  of  Pseudopodia 156 

Movements  at  Anterior  Edge 160 

Lack  of  Backward  Currents 134        Movements  of  Posterior  Part  of  Body. ...  165 

Movements  of  Upper  and  Lower  Surfaces  General  View  of  Movements  of  Amoeba  in 

Studied   Experimentally;     Rolling  Locomotion 169 

Movement 138        Some  Characteristics  of  the  Substance  of 

Amceia  verrucosa  Sind  Its  Rclsitives.  140  Amoeba 173 

Other  Species  of  Amoeba 146  Fluidity 173 

Historical  on  Rolling  Movements  in  Rhumbler's  Ento-ectoplasm  Process  173 


Amoeba 148 


Elasticity  of  Form  in  Amoeba 175 

Contractility  in  Ectosarc  of  Amoeba.  177 

Reactions  to  Stimuli 181 

Reactions  to  Mechanical  Stimuli 181        Some  Complex  Activities 193 

Positive  Reaction 181  Activities  connected  with  Food-taking  193 

Negative  Reaction 182  Taking  Food ^ 193 

Reaction  to  Chemical  Stimuli 187  Pursuit  of  Food 196 

Reaction  to  Heat 190  Other  Amcebse  as  Food 198 

Reactions  to  Other  Simple  Stimuli 191  Reactions  to  Injuries 202 

Physical  Theories  and  Physical  Imitations  of  Amoeboid  Movements,        .     204 

Surface  Tension  Theory 204  Experimental    Imitation    of  Movements 

Berthold's  Theory  that  One-sided  Adher-  due  to  Local  Contractions  of  Ectosarc 

ence  to  Substratum  is  the  Cause  of  and  of  the  Roughening  of  Ectosarc  in 

Locomotion 208  Contraction 215 

Experimental  Imitation  of  Locomo-  Direct  or    Indirect  Action   of   External 

tion  in  Amoeba 209  Agents  in  Modifying  Movements 219 

Formation  of  Free  Pseudopodia 214  Direct  or  Indirect  Action  in  Food-taking,  222 

General  Conclusion 225 

Behavior  of  Amoeba  from  Standpoint  of  Comparative  Study  of  Animal 

Behavior 226 

Habits  in  Amoeba 226        Relation  of  Different  Reactions  to  Differ- 

Classes  of  Stimuli  to  which  Amoeba  Re-  ent  Stimuli;    Adaptation  in  Beha- 

acts 227  vior  of  Amoeba 227 

Types  of  Reaction 227        Reflexes  and   "Automatic  Actions"   in 

Amoeba 228 

Variability  and  Modifiability  of  Reactions  229 

Summary,    .        .        ,        , 230 

130 


THE   MOVEMENTS   AND    REACTIONS    OF  AMCEBA. 


INTRODUCTION;   OBJECTS  OF  THE  INVESTIGATION. 

The  present  paper  contains  the  results  of  an  investigation  which  was 
undertaken  with  two  general  problems  in  mind.  The  first  purpose 
was  to  determine  by  observation  and  experiment,  from  the  standpoint 
of  the  student  of  animal  behavior,  how  far  recent  physical  and 
mechanical  theories  go  in  aiding  us  to  explain  the  behavior  of  Amoeba. 
The  second  object  of  the  work  was  to  furnish  needed  additional  data 
on  the  reactions  of  i\.moeba  to  stimuli,  and  to  systematize  and  unify 
our  knowledge  of  its  behavior. 

The  recent  theories  which  would  resolve  the  activities  of  Amoeba 
largely  into  phenomena  due  to  alterations  in  the  surface  tension  of  a 
complex  fluid  seem  to  promise  much.  They  are  of  precisely  the 
character  from  which  most  may  be  hoped  ;  from  a  study  of  the  physics 
of  matter  in  a  state  similar  to  that  found  in  the  living  substance,  the 
laws  of  action  of  this  living  substance  are  sought.  Such  theories  have 
been  developed,  as  is  well  known,  by  Berthold  (1886),  Quincke 
(1S8S),  Biitschli  (1892),  Verworn  (1892),  Rhumbler  (1898),  Bern- 
stein (1900),  Jensen  (1901),  and  others.  The  success  of  this  method 
of  attacking  the  problems  seems  great.  Activities  similar,  at  least 
externally,  to  those  of  Amoeba,  are  produced  by  physical  means,  and 
fully  analyzed  from  the  physical  and  mechanical  standpoint.  In  this 
manner  the  movement,  the  control  of  movement  by  external  agents, 
the  feeding,  the  choice  of  food,  the  making  of  the  shell,  and  other 
features  of  the  behavior  have  been  more  or  less  closely  imitated,*  and 
in  a  way  permitting  a  complete  analysis  in  accordance  with  chemical 
and  physical  laws. 

From  the  standpoint  of  the  student  of  animal  behavior,  the  resolu- 
tion of  the  behavior  of  any  organism  into  the  action  of  known  physical 
laws  must  be  a  matter  of  the  deepest  interest.  The  actions  of  higher 
organisms  seem  at  present  so  far  from  such  a  resolution  that  some 
investigators  believe  an  essential  difference  in  principle  to  exist 
between  the  behavior  of  living  things  and  non-living  things ;  between 
the  laws  of  biology  and  those  of  physics.  The  resolution,  then,  of  the 
behavior  of  even  the  simplest  organism  into  known  physical  factors 
would  be  an  event  of  capital  significance,  affecting  fundamentally  the 
whole  theory  of  animal  behavior.     A  renewed  thorough  study  of  the 


*  See  especially  Rhumbler,  1898.  131 


132  THE    BEHAVIOR   OF   LOWER   ORGANISMS. 

facts,  with  especial  reference  to  these  theories,  seems,  therefore,  much 
to  be  desired.  The^  results  of  the  present  study  will  show,  I  believe, 
that  such  a  re-examination  of  the  fjicts  was  greatly  needed. 

As  to  the  second  object  of  this  investigation,  stated  above,  it  is  a 
somewhat  remarkable  fact  that  the  observational  basis  for  a  number  of 
the  most  important  reactions  assumed  to  exist  in  Amoeba  is  exceedingly 
scanty,  particularly  so  far  as  control  of  the  direction  of  movement  is 
concerned.  For  example,  one  of  the  reactions  most  often  assumed  to 
exist  in  Amoeba,  and  most  commonly  selected  for  imitation  by 
physical  means,  is  chemotaxis,  the  movement  toward  or  away  from  a 
diffusing  chemical.  But  no  account  exists,  so  far  as  I  have  been  able 
to  discover,  of  actual  observation  of  such  a  reaction  in  Amoeba,  under 
experimental  conditions.  Again,  the  effects  of  slight  or  of  intense 
localized  mechanical  stimuli,  in  controlling  the  direction  of  movement, 
has  not  been  worked  out  in  detail.  To  fill  these  and  similar  gaps  in 
our  knowledge,  and  to  bring  the  different  reactions  into  relation  with 
each  other,  so  as  to  make  possible  a  connected  account  of  the  behavior 
of  Amoeba,  is,  then,  the  second  object  of  this  paper. 

I  shall  first  give  an  account  of  the  movements  and  reactions  of 
Amoeba,  as  determined  by  observation  and  experiment,  without  enter- 
ing in  detail  upon  the  theories  of  the  subject.  This  will  be  followed 
by  a  section  dealing  with  the  physical  theories  and  physical  imitations 
of  the  movements  and  reactions,  in  the  light  of  the  facts  set  forth  in  the 
first  section.  A  brief  final  section  will  be  devoted  to  a  characterization 
of  the  behavior  of  Amoeba  from  the  standpoint  of  the  student  of 
animal  behavior. 

I  am  compelled  to  give  a  full  description  of  the  normal  movements 
of  Amoeba,  as  the  course  of  the  investigation  showed  that  the  prevalent 
conception  of  these  movements,  on  which  many  of  the  theories  have 
been  based,  is  not  correct. 

DESCRIPTION  OF  THE  MOVEMENTS  AND   REACTIONS. 
THE  MOVEMENTS. 
MOVEMENTS  OF  AMCEBA  AS  DESCRIBED    BY  RHUMBLER  AND  BUTSCHLI  ; 
AGREEMENT  WITH  CURRENTS  IN  A  DROP  OF  FLUID  MOVING  AS  A  RE- 
SULT OF  LOCAL  DECREASE  IN  SURFACE  TENSION. 

There  are  few  subjects  that  have  been  studied  more  than  the  nature 
of  the  movements  of  Amoeba,  but  nothing  final  has  been  reached,  even 
from  the  descriptive  standpoint.  The  first  preliminary  to  an  under- 
standing of  the  nature  of  the  movements  must  be  to  determine  just  what 
movements  take  place. 

The  most  extensive  recent  study  of  the  movements  of  Amoeba  has 
been  made  by  Rhumbler  (1898),  though  the  magnificent  monograph  of 


THE    MOVEMENTS   AND    REACTIONS   OF   AMOBBA. 


133 


the  Rhizopods  by  Penard  (1902)  contains  incidentally  a  large  number 
of  valuable  observations  on  this  matter. 

According  to  Rhumbler  (/.  c.)  the  movements  in  normal  locomotion 
are  typically  as  follows  :  From  the  hinder  end  of  the  Amoeba  (or  of  the 
pseudopodium,  if  a  single  pseudopodium  is  under  consideration)  a 
current  of  endosarc  passes  forward  in  the  middle  axis  ;  in  front  this  flows 
outward  toward  the  sides,  then  backward  along  the  surface,  gradually 
coming  to  rest.  Figs.  30  and  31 ,  taken  from  Rhumbler,  give  diagrams 
of  these  currents  in  an  Amoeba  moving  as  a  whole  (Fig.  30),  and  in 
the  formation  of  pseudopodia  (Fig.  31).  In  an  Amoeba  which  forms 
more  than  one  pseudopodium  at  once,  these  typical  currents  become 
somewhat  complicated  (Fig.  32),  but  retain  their  main  features.  The 
backward  current  shown  at  the  sides  in  Figs.  30-32  is  conceived  to  be 
present  also  above  and  below,  that  is,  over  the  whole  surface  of  the 
Amoeba.  A  diagram  of  the  currents  in  side  view,  as  given  by  Rhum- 
bler, is  shown  in  Fig.  33,  B.  An  essentially  similar  account  of  the 
currents  is  given  by  Biitschli  (1880,  1892). 


Fig.  30.* 


Fig.  31. t 


Fig.  32.  t 


Fig.  33.§ 


The  most  striking  feature  in  the  currents  as  above  set  forth  is  the  fact 
that  they  agree  precisely  with  the  currents  produced  in  a  drop  of  fluid 
of  any  sort  when  the  surface  tension  is  lowered  over  a  certain  limited 
area.  There  is  always  a  current  over  the  surface  away  from  the  region 
where  the  tension  is  lowered,  while  an  axial  current  moves  toward  the 


♦Fig.  30. — Diagram  of  the  currents  in  a  progressing  Amoeba  Umax,  after 
Rhumbler  (1898). 

fFiG.  31. — Diagram  of  the  **  fountain  currents  "  in  pseudopodia  of  Amceba, 
after  Rhumbler  (1898). 

%  Fig.  32. — Diagram  of  complex  '*  fountain  currents"  in  an  Amoeba  with  two 
large  pseudopodia,  after  Rhumbler  (1898). 

§  Fig.  33. — Comparative  diagrams  of  the  currents  in  a  rolling  movement,  and 
in  the  movement  of  Amoeba,  as  conceived  by  Rhumbler,  viewed  from  the  side. 
In  A  are  represented  what  Rhumbler  conceives  to  be  the  necessary  currents  in 
a  rolling  movement,  while  B  represents  what  Rhumbler  considers  the  really 
existing  currents  in  Amoeba,  as  seen  from  the  side.  The  heavier  arrows  in  each 
case  represent  the  current  on  the  lower  surface.    After  Rhumbler  (1898). 


134  "^"^    BEHAVIOR    OF    LOWER    ORGANISMS. 

point  of  lowered  tension.  Diagrams  of  the  movement  of  such  drops 
are  given  in  Fig.  34.  Further,  the  drop  may  elongate  in  the  direction 
of  the  axial  current,  and  may  move  bodily  in  that  direction,  just  as 
happens  in  Amoeba.*  It  is  most  natural,  therefore,  to  conclude  as 
Biitschli  (1892)  and  Rhumbler  (1898)  have  done,  that  the  movements 
of  Amoeba  are  likewise  due  to  a  lowering  of  the  surface  tension  at  the 
anterior  end,  provided  that  its  movements  really  take  -place  in  the 
way  described  above, 

CURRENTS  IN  AMCEBA  AS  STUDIED  FROM  ABOVE  ;  LACK  OF  BACKWARD 

CURRENTS. 

At  the  beginning  of  my  work  I  had  no  doubt  that  the  movements 
occurred  exactly  as  above  described,  and,  therefore,  did  not  devote 
special  attention  to  this  point.  But  I  was  soon  struck  by  the  fact  that 
I  was  unable  to  see  any  backward  current  at  the  sides,  as  represented 
in  Figs.  30  and  31.  Further  careful  study  of  the  movements  of 
Amoeba  limax^  A.  proteus^  A.  angulata^  A.  verrucosa^  A,  sphcero- 

nucleolus,,  and  one  or  two 
undetermined  species 
confirmed  this  fact,  and  I 
may  say  at  once  that  after 
several  months'  continu- 
-^  F  +         ^  ^"^  study  of  the    move- 

ments and  reactions  of 
Amoeba  I  have  never,  except  in  one  or  two  doubtful  instances,  seen 
any  backward  movement  of  the  substance  at  the  sides  or  on  the  surface 
of  an  Amoeba  that  was  moving  forward  in  a  definite  direction. 

It  is  true  that  in  the  movements  of  Amoeba  limax^  for  example,  one 
receives  the  impression  of  two  sets  of  currents,  one  forward  in  the  cen- 
tral axis,  the  other  backward  at  the  sides.  But  if  the  latter  is  studied 
carefully  it  is  found  that  there  is  really  no  current  here ;  the  proto- 
plasm is  at  rest,  and  the  impression  of  a  backward  current  at  the  sides 
is  produced  only  by  contrast  with  the  forward  axial  current.     Amoeba 


♦All  these  facts  are  easily  verified  bj  placing  a  drop  of  clove  oil  on  a  slide  in 
a  mixture  of  two  parts  glycerine  to  one  part  95  per  cent  alcohol  under  a  cover 
supported  by  glass  rods,  as  described  in  a  previous  paper  by  the  present  author 
(Jennings,  1902).  By  mixing  some  soot  or  India  ink  with  the  clove  oil  the  cur- 
rents are  made  evident. 

t  Fig.  34. — Currents  in  a  drop  of  fluid  when  the  surface  tension  is  decreased 
on  one  side.  A,  the  currents  in  a  suspended  drop,  when  the  surface  tension  is 
decreased  at  a.  After  Berthold  (1886).  ^,  axial  and  surface  currents  in  a  drop 
of  clove  oil,  in  which  the  surface  tension  is  decreased  at  the  side  a.  The  drop 
elongates  and  moves  in  the  direction  of  a,  so  that  an  anterior  (a)  and  a  posterior 
(^)  end  are  distinguishable. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  1 35 

Umax  contains  usually  a  large  number  of  fine  granules,  which  in  many 
cases  extend  to  the  very  outer  surface,  so  that  it  is  not  possible  to  dis- 
tinguish an  ectosarc,  in  the  sense  of  a  layer  containing  no  granules. 
By  watching  the  movements  of  these  particles  it  is  possible  to  determine 
the  direction  of  the  currents  in  the  protoplasm.  The  movements  in 
locomotion  are  usually  as  follows :  At  the  anterior  end  there  pushes 
forth  from  the  interior  a  clear  substance,  which  I  will  call  the 
hyaloplasm.  As  this  moves  forward  it  spreads  out  laterally,  till  it 
reaches  a  position  such  that  it  forms  a  continuation  forward  of  the 
remainder  of  the  lateral  boundary  of  the  animal.  Into  this  hyaloplasm 
flows  then  the  granular  endosarc.  The  granules  flow  forward,  rapidly 
in  the  middle,  usually  more  slowly  near  the  sides.  As  it  reaches  the 
anterior  end  the  central  current  spreads  out  in  a  fanlike  manner,  so 
that  some  of  the  granules  approach  closely  the  lateral  borders  of  the 
Amoeba  (Fig.  35).  They  then  stop,  while  the  central  part  of  the  cur- 
rent passes  on,  following  the  advancing  anterior  end. 

So  long  as  one  confines  his  attention  to  the  Amoeba  alone,  not 
observing  external  objects, 
one  receives  the  impres- 
sion that  there  are  two 
sets  of  currents,  an  axial 
current  forward,  marginal 

currents  backward.     But 

a         !-•  Fig.  ^c.* 

as  soon  as  one  fixes  his  ^^ 

eye  upon  a  particular  granule  in  the  apparent  backward  marginal 
current,  and  observes  its  relation  to  some  external  object,  he  dis- 
covers that  no  such  current  exists.  The  granule  remains  quiet, 
retaining  continually  its  position  with  relation  both  to  other  granules 
in  the  edge  of  the  Amoeba  and  to  objects  external  to  the  Amoeba. 
Meanwhile  the  remainder  of  the  substance  of  the  Amoeba  is  flowing 
past,  so  that  the  granule  in  question  after  a  time  comes  to  occupy 
a  position  at  the  middle  of  the  length  of  the  Amoeba.  At  about 
this  point  it  usually  begins  to  move  slowly  forward  again,  though 
much  less  rapidly  than  the  internal  current.  The  nature  of  this 
slow  forward  movement  we  shall  take  up  later  (p.  166).  The  main 
portion  of  the  body  of  the  Amoeba  thus  continues  to  pass  the  granule, 
and  the  latter  finally  reaches  the  posterior  end.  Here  it  usually  re- 
mains quiet  for  a  time  (moving  forward  only  as  the  posterior  end  is 
dragged  forward).  Then  it  is  taken  into  the  central  current  again, 
passes  to  the  anterior  end,  and  comes  to  rest  as  before,  while  the 
remainder  of  the  Amoeba  passes  it  by ;  and  this  process  is  repeated 

*  Fig.  35. — Diagram  of  the  movements  of  particles  in  an  advancing  Amoeba. 
Each  broken  line  represents  the  path  of  a  particular  particle. 


136  THE   BEHAVIOR   OF   LOWER    ORGANISMS. 

indefinitely.  In  favorable  cases  I  have  repeatedly  followed  a  single 
granule  from  the  posterior  end  forward  till  it  came  to  rest  at  the 
anterior  end,  then  watched  the  body  of  the  Amoeba  pass  it  by,  until  it 
was  again  at  the  posterior  end  and  started  forward  anew.  The  course 
of  a  single  granule  is  represented  in  Fig.  36.  As  is  evident  from  this 
figure,  the  granule  does  not  travel  backward  in  any  part  of  its  course. 
Not  all  the  granules,  however,  remain  quiet  until  they  have  passed  to 
the  posterior  end.  Many  of  them  are  taken  again  into  the  central 
stream  before  the  entire  body  of  the  Amoeba  has  passed  them.  Large 
granules  usually  stop  only  a  short  time,  starting  forward  again  before 
the  middle  of  the  Amoeba  has  reached  them  ;  others  are  taken  up  at  the 
middle  or  farther  back,  while  many  smaller  granules  reach  the  posterior 
end.  But  as  a  rule  none  show  any  movement  backward,  so  far  as  I 
have  observed. 

It  is  not  only  at  the  margins  of  the  Amoeba,  but  also  on  the  under 
surface,  in  contact  with  the  substratum,  that  the  ectosarc  with  its 
granules  is  at  rest  or  moving  slowly  forward  in  the  posterior  half. 
This  is  evident  when  the  lower  surface  of  a  transparent  Amoeba  is 
brought  into  focus. 

^  2  That  excellent  observer, 

i  -'x^ ..^    Dr.  Wallich,  saw  clearly 

/"^ — ,^-;?<^ — "^^  fS^ — ZXA-*- cy.         J     many  years  ago  that  there 

Vj-^ — ~^i_^-{ — ~3p^-=r^^:^^'-f^L,^__J    A     is  really  no  backward  cur- 

o.  ^  'c  "^  e        J    rent,  though  at  first  view 

Fig.  36.*  there  appears  to  be  such. 

It  is  only  necessary  to  watch  a  specimen  of  Amoeba  carefully  to  become  con- 
vinced that  the  appearance  of  a  returning,  as  well  as  an  advancing,  stream  of 
granules  is  illusory.  The  stream,  it  will  be  observed,  is  invariably  in  the  direc- 
tion of  the  preponderating  pseudopodial  projections.  The  particles  simply  flow 
along  with  the  advancing  rush  of  protoplasm.  There  is  no  return  stream,  but 
the  semblance  of  one  is  engendered  by  one  layer  of  particles  remaining  at  rest 
whilst  another  is  moving  past  them.     (Wallich,  1863,  b,  p.  331.) 

This  statement  of  the  facts  my  observations  fully  confirm. 
In  this  account  of  the  lack  of  backward  movement  in  the  granules 
of  the  ectosarc  on  the  lower  surface  and  at  the  margins  I  find  myself 


♦Fig.  36. — Diagram  of  the  movements  of  a  single  particle  in  Amoeba,  as 
seen  from  above.  The  particle  begins  at  a,  passes  to  b  and  then  to  c,  at  the 
anterior  edge  of  the  Amoeba  shown  in  the  outline  i.  The  Amoeba  now  passes 
forward  to  the  position  2,  and  thence  to  3,  while  the  particle  retains  the  posi- 
tion c;  when  the  Amoeba  has  reached  the  position  3  the  particle  is  thus  at 
its  posterior  end.  Now  the  particle  moves  forward  again,  from  c  to  d,  and 
thence  to  e  and/",  thus  coming  again  to  the  anterior  edge.  Here  it  stops,  as  at 
c,  until  the  body  of  the  Amoeba  has  passed  it.  As  the  figure  shows,  the  particle 
does  not  move  backward  in  any  part  of  its  course. 


THE    MOVEMENTS   AND   REACTIONS    OF   AMCEBA.  I37 

at  variance  with  certain  statements  of  F.  E.  Schulze,  Biitschli,  and 
Rhumbler.  I  am  aware  that  this  conflict  of  my  observations  with 
those  of  the  investigators  named,  who  deservedly  rank  among  the 
highest  in  the  field  at  present  under  consideration  as  well  as  elsewhere, 
renders  the  utmost  caution  necessary  in  trusting  to  these  results.  Yet, 
with  this  consideration  in  mind,  and  with  the  confident  expectation  in 
undertaking  the  work  that  I  should  find  the  currents  exactly  as  described 
by  these  authors,  I  have  been  unable  to  come  to  any  result  save  that 
above  set  forth.  The  statements  of  Schulze  (1875,  pp.  344-348)  deal 
with  Pelomyxa  falustris  Greef.  In  this  animal,  according  to  Schulze, 
there  are  resting  portions  at  the  sides  of  the  body,  while  from  behind 
currents  pass  forward  through  the  channel  enclosed  by  these  resting 
portions.  At  the  anterior  end  the  lateral  parts  of  these  currents  turn 
outward  and,  finally,  a  little  backward ;  any 
given  portion  passes  backward  but  a  short  dis- 
tance. The  currents  are  shown  by  Schulze  in 
a  figure,  a  reduced  copy  of  which  is  given  here- 
with (Fig.  37).  According  to  Schulze  the  cur- 
rents have  this  form  on  the  upper  surface  as  well  '^^"^■***''^'^^^^^^'f^^  V^—x 
as  at  the  sides — that  is,  a  part  of  the  current  flows 
upward  and  backward  on  the  upper  surface. 
Biitschli  (1892,  Anhang,  p.  220)  confirms  this 
account  of  the  currents  in  Pelomyxa. 

I  regret  that  I  have  been  unable  to  obtain 
specimens  of  Pelomyxa  in  order  to  examine 
these  phenomena  for  myself.  One  would  of 
course  be  bold  to  doubt  the  correctness  of  the 

KiG     Vl  * 

observations  of  such   investigators    as    Schulze 

and  Biitschli,  and  it  is  possible  that  Pelomyxa  differs  from  Amoeba 
in  this  respect.  Yet,  as  we  shall  see  later  (p.  149),  the  account  given 
by  these  authors  is  certainly  incorrect  so  far  as  the  backward  cur- 
rents on  the  upper  surface  are  concerned  ;  it  is  possible,  then,  that  the 
appearance  of  a  backward  current  elsewhere  was  deceptive. 

Rhumbler  (1898)  describes  the  forward  axial  and  the  backward  side 
currents  in  various  species  of  Amoeba,  and  considers  such  movements 
as  typical,  basing  his  theory  of  locomotion  upon  them.  It  seems 
probable  that  slight  backward,  currents,  such  as  were  described  by 
Schulze  (Fig.  37),  do  occur  at  times  at  the  sides  of  the  advancing 
anterior  end.  The  posterior  part  of  the  Amoeba  is  narrow  and 
rounded,  the  anterior  part  broad  and  thin.  The  current  of  endosarc 
flows  from  this  narrow  posterior  portion  into  the  broad  anterior  part 

♦Fig.  37. — Currents  in  a  progressing  Pelomjxa,  as  seen  from  above,  after 
Schulze  (1875).    The  longer  arrows  represent  stronger  currents. 


138  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

and  must  therefore  spread  out ;  it  would  not  be  unnatural  for  the 
currents  to  flow  even  backward  a  little,  as  in  Schulze's  figure  (Fig. 
37),  in  order  to  fill  the  area  just  in  front  of  the  resting  portion  of  the 
protoplasm  (at  x,  Fig.  37).  As  we  shall  see,  such  movement  is 
sometimes  to  be  observed  in  inorganic  fluids  under  similar  conditions 
(p.  211).  Whatever  the  explanation  of  the  difference  between  my 
observations  and  those  of  the  investigators  named,  the  point  of  impor- 
tance is  that  the  backward  current  is  not  a  constant  nor  an  essential 
part  of  the  locomotion  of  Amoeba,  so  that  it  does  not  form  a  fitting 
basis  for  a  theory  of  locomotion.  Further,  as  we  shall  see,  I  am  able 
to  demonstrate  conclusively  the  incorrectness  of  that  conception  of  the 
nature  of  amoeboid  movement  for  which  alone  the  account  of  the 
currents  given  by  Biitschli  and  Rhumbler  is  significant. 

It  is  evident  that  the  method  of  movement  here  described  is  better 
adapted  to  the  production  of  locomotion  in  a  given  direction  than  that 
which  Biitschli  and  Rhumbler  describe  (see  Figs.  30-33),  since  accord- 
ing to  their  account  a  portion  of  the  substance  of  the  body  is  first  trans- 
ported forward,  then  backward.  In  the  locomotion  as  I  observed  it 
there  is  no  such  useless  transportation  of  substance  in  a  direction 
opposed  to  that  in  which  the  animal  is  traveling. 

On  the  other  hand,  the  movements  as  I  have  described  them  bear 
much  less  resemblance  to  those  produced  in  drops  of  fluid  by  local 
changes  in  surface  tension  (Fig.  34) .  There  is  only  the  slight  turning 
outward  at  the  anterior  end  that  can  be  at  all  compared  to  the  backward 
flow  of  an  outer  layer  in  the  inorganic  drop.  Rhumbler  himself  notes 
that  in  Amoeba  angulata  there  is  often  no  such  backward  current  to 
be  seen  (Rhumbler,  1898,  p.  120),  but  bases  his  theory  of  the  forward 
movement  entirely  on  the  cases  where  it  (supposedly)  does  occur.  In 
Amceba  angulata^  A.  verrucosa^  and  A.  sphceronucleolus^  according 
to  my  observations,  there  is  often  no  indication  even  of  the  turning 
out  of  the  particles  in  a  fanlike  manner  ;  they  merely  flow  forward  and 
stop  for  a  time.  Biitschli  (1892,  p.  199)  notes  that  the  backward  cur- 
rent at  the  anterior  end  of  Amoeba,  required  by  the  surface  tension 
theory,  is  very  slight,  but  conceives  it  to  be  suflicient  to  fulfill  the 
requirements  of  the  theory. 

MOVEMENTS    OF    UPPER    AND    LOWER    SURFACES  STUDIED  EXPERIMEN- 
TALLY  ROLLING  MOVEMENT  IN  AMCEBA. 

Thus  far  we  have  left  out  of  consideration  the  movement  of  substance 
on  the  upper  surface  of  the  Amoeba.  It  is  usually  assumed  that  the 
condition  here  is  the  same  as  at  the  sides  and  on  the  under  surface ; 
thus  Rhumbler  gives  a  diagram,  reproduced  in  my  Fig.  33,  B^  showing 
the  backward  current  of  the  upper  surface.     The  positive  observations 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I39 

on  this  point  are  those  of  Schulze  (1875),  Berthold  (1886,  p.  109),  and 
Biitschli  (1892,  p.  220).  These  authors  all  agree  that  the  backward 
current  visible  at  the  sides  of  the  anterior  end  in  Pelomyxa  are  clearly 
also  present  on  the  upper  surface.  It  is  not  usually  possible  to  observe 
particles  moving  backwrard  on  the  upper  surface  of  Amceba,  nor  even 
particles  at  rest,  though  this  might  be  due  to  the  fact  that  the  granules 
have  sunken  downward,  leaving  the  upper  surface  clear.  But  to 
decide  whether  the  currents  in  Amoeba  are  essentially  like  those  pro- 
duced in  a  drop  of  fluid  by  a  local  change  in  surface  tension,  it  is  most 
important  to  determine  with  certainty  what  is  taking  place  on  the  upper 
surface. 

Evidently  the  most  natural  way  of  doing  this  is  to  cause,  if  possible, 
some  small  object  to  rest  upon  or  become  attached  to  the  upper  surface 
of  Amceba,  then  to  observe  the  movement  of  this  object.  This  can  be 
done  by  mingling  a  considerable  quantity  of  soot  with  the  water  in 
which  the  Amoebae  are  found.    Some  of  the  soot  particles  settle  on  the 


Fig.  38.*  Fig.  39.! 

upper  surface  of  the  Amoebae,  and  in  some  species  they  adhere  to  this 
surface. 

I  was  quite  unprepared  for  the  results  of  this  experiment.  The 
upper  surface  of  Amceba  moves  forward^  not  backward,  as  required 
by  the  surface  tension  theory ;  nor  is  it  at  rest  like  the  lower  surface. 


*  Fig.  38. — Movements  of  a  particle  attached  to  the  outer  surface  of  Amoeba 
verrucosa.  When  first  seen  the  particle  was  at  the  posterior  end  {p) ;  it  then 
moved  forward,  as  shown  by  the  arrows,  until  it  passed  around  the  anterior  end 
(a)  to  the  under  side.  (The  Amceba  itself  of  course  moved  forward  at  the  same 
time;  no  attempt  is  made  to  represent  its  movement  in  the  figure.) 

t  Fig.  39. — Diagram  of  the  movements  of  a  particle  attached  to  the  outer 
surface  o(  Amoeba  verrucosa,  in  relation  to  the  movements  of  the  animal.  The 
Amoeba  is  seen  from  above.  In  the  position  i  the  particle  is  at  the  anterior  end 
of  the  Amoeba.  As  the  Amoeba  moves  forward,  it  passes  over  the  particle, 
which  retains  its  place.  Thus  when  the  Amoeba  has  reached  the  position  2  the 
particle  is  at  the  middle  of  its  lower  surface;  when  it  reaches  3  the  particle  is  at 
its  posterior  end.  The  particle  then  passes  upward  and  forward,  as  shown  by 
the  arrows,  so  that  when  the  Amoeba  reaches  the  position  4  the  particle  is  in 
front  of  the  middle,  on  the  upper  surface. 


140  THE   BEHAVIOR   OF   LOWER   ORGANISMS. 

AMCEBA   VERRUCOSA   AND    ITS    RELATIVES. 

In  giving  an  account  of  the  experiments  which  demonstrate  this,  I 
shall  begin  with  species  of  Amoeba  in  which  pseudopodia  are,  as  a  rule, 
not  formed,  and  the  movements  are  uniform  in  character,  since  here  the 
conditions  are  simplest  from  our  present  standpoint.  For  this  purpose 
Amoeba  verrucosa  Ehr.,  and  particularly  the  transparent  form  known 
as  A.  sphceronucleolus  Greef,  are  favorable.  In  these  Amosbae  particles 
cling  rather  easily  to  the  outer  surface. 

When  a  quantity  of  soot  is  added  to  the  water  containing  Amoebae 
of  the  species  named,  small  masses  cling  to  the  surface  of  the  animal. 
Such  a  mass,  attached  to  the  upper  surface,  shows  the  following 
movements  :  It  passes  slowly  forward  (Fig.  38) ,  then  over  the  anterior 
edge,  and  under  the  latter.  Here  it  stops,  while  the  Amoeba  continues 
to  move  forward.  The  mass  of  soot  remains  quiet  until  the  entire 
Amoeba  has  passed  over  it  and  it  lies  beneath  the  posterior  end.  It 
now  passes  upward  again,  to  the  upper  surface  (Figs.  39,  40),  then 
forward  once  more  to  the  anterior  end.     Here  it  goes  under  the  Amoeba 


as  before,  to  be  carried  upward  and  forward  again  when  the  posterior 
end  passes  over  it. 

These  observations  are  made  with  absolute  ease,  and  there  is  no  pos- 
sibility of  mistaking  internal  particles  for  external  ones.  Particles  lying 
in  the  water  outside  the  Amoeba  may  be  seen  to  become  attached  at  the 
posterior  end,  to  pass  upward,  lying  distinctly  outside  the  boundary  of 
the  protoplasm  (Fig.  38,  posterior  end),  then  forward,  till  as  they  double 
the  anterior  end  they  are  again  seen  sharply  defined  outside  the  boundary 


♦  Fig.  40. — Diagram  of  the  movements  of  a  particle  attached  to  the  surface  of 
Amoeba  verrucosa,  in  side  view.  In  position  i  the  particle  is  at  the  posterior 
end;  as  the  Amoeba  progresses  it  moves  forward,  as  shown  at  2,  and  when  the 
Amoeba  has  reached  the  position  3  the  particle  is  at  its  anterior  edge,  at  x. 
Here  it  is  rolled  under  and  remains  in  position,  so  that  when  the  Amoeba  has 
reached  the  position  4  the  particle  is  still  at  x,  at  the  middle  of  its  lower  surface. 
In  the  position  5  the  particle  is  still  in  the  same  place,  *,  save  that  it  is  lifted 
upward  a  little  as  the  posterior  end  of  the  Amoeba  becomes  free  from  the  sub- 
stratum. Now  as  the  Amoeba  passes  forward  the  particle  is  carried  to  the  upper 
surface,  as  shown  at  6.  (Thence  it  continues  forward  and  again  passes  beneath 
the  Amoeba,  etc.)  The  broken  lines  show  that  part  of  the  surface  of  the  Amoeba 
which  is  at  rest. 


THE    MOVEMENTS   AND   REACTIONS   OF   AMCEBA.  I4I 

(Fig.  38,  anterior  end).     Further,  such  particles,  after  making  one  or 
two  revolutions,  usually  become  detached  and  drop  off. 

It  is  thus  clear  that  Amoeba  verrucosa  and  its  relatives  have  what 
may  be  called  a  rolling  motion  ;  a  given  spot  on  the  outer  pellicula 
passes  forward  on  the  upper  surface,  downward  at  the  anterior  end, 
remains  quiet  on  the  lower  surface,  passes  upward  at  the  posterior 
end,  and  again  forward.  Its  movement  may  be  compared  directly  with 
the  movement  of  a  given  point  on  the  circumference  of  a  wheel  that  is 
rolling  forward.  A  diagram  of  the  movement  of  a  particle  on  the 
surface  as  it  would  appear  in  a  side  view  is  given  in  Fig.  40. 

Certain  details  of  the  movements  are  interesting,  and  may  best  be 
brought  out  by  description  of  specific  observations.  In  one  case  two 
small  particles  had  become  attached,  a  short  distance  apart,  to  the  surface 
of  a  specimen  of  Amoeba  spkceronucleolus.  They  were  at  first  side  by 
side  and  a  little  to  the  right  of  the  middle  line,  one  somewhat  farther 
to  the  right  than  the  other  (Fig.  41) .  They  moved  forward  in  parallel 
courses,  and  reached  the  anterior  edge  at  the 
same  time,  passing  over  the  edge  and  to  the 
under  surface.  It  now  required  two  and  one- 
half  minutes  for  the  Amoeba  to  pass  over  p 
them,  during  which  time  they  remained  nearly 
or  quite  at  rest.  They  then  moved  upward 
to  the  upper  surface  and  forward  again.     The  ^  ^ 

one  nearer  the  middle  line  moved  a  little 
faster  than  the  other,  reaching  the  anterior  edge  in  two  and  three- 
quarter  minutes,  while  the  lateral  one  required  three  minutes.  Both 
emerged  at  the  posterior  end  again  at  the  same  time,  the  central 
one  having  remained  quiet  three  and  one-fourth  minutes,  while  the 
lateral  one  had  been  three  minutes  at  rest.  The  next  forward  course 
required,  respectively,  but  one  and  one-half  and  two  minutes,  the  central 
particle  movmg  the  more  rapidly.  The  two  particles  were  no  longer 
side  by  side,  the  central  one  being  now  a  little  in  advance.  The  latter 
spent  after  the  next  turn  two  and  one-half  minutes  on  the  under  surface, 
while  the  lateral  particle  spent  but  two  minutes,  so  that  they  came  up 
from  the  posterior  end  again  at  the  same  time. 

The  two  particles  started  forward  again  and  had  reached  the  middle 
of  the  upper  surface  when  the  Amoeba  ceased  its  forward  movement, 
loosened  its  anterior  end  from  the  bottom,  and  became  attached  by  its 
posterior  end.     After  five  minutes  it  began  to  move  again,  but  now  in 


♦Fig.  41. — Paths  of  two  particles  attached  to  the  outer  surface  of  Amoeba, 
sphcerottucleolus  as  described  in  the  text.  That  portion  of  the  paths  which  is  on 
the  lower  surface  is  represented  by  broken  lines.  (No  attempt  is  made  to  rep- 
resent the  forward  movement  of  the  Amceba  in  this  fij^re.) 


142  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

the  opposite  direction,  so  that  the  former  posterior  end  became  anterior. 
At  the  same  time  the  two  particles  reversed  their  former  motion  and 
began  to  travel  back  in  the  direction  from  which  they  had  come — that 
is,  toward  the  new  anterior  end.  They  were  observed  to  make  several 
complete  turns  about  the  Amoeba  while  moving  in  this  new  direction. 
I  will  not,  however,  add  further  details,  as  those  above  recounted  are 
sufficient  to  give  a  conception  of  the  main  features  of  the  movement. 

Thus  two  definite  points  on  the  surface  of  an  Amoeba  may  retain 
nearly  the  same  relation  to  one  another  for  five  or  six  complete  revolu- 
tions, though  their  distance  apart  and  their  relative  position  may  vary 
a  little.  The  reversal  of  the  direction  of  rotation  when  the  direction  of 
locomotion  is  reversed,  described  in  the  above  case,  I  have  seen  many 
times. 

The  direction  of  the  movement  of  particles  on  the  outer  surface  is 
the  same  as  that  of  the  underlying  particles  of  endosarc.  The  rate  is 
also  about  the  same  as  for  the  endosarc,  though  often,  or  perhaps 
usually,  the  outer  particles  move  a  little  more  slowjy  than  those  in  the 
endosarc. 

It  is  not  merely  a  thin  outer  layer  that  has  the  rolling  movement. 
This  is  demonstrated  by  the  movements  of  bodies  that  are  partly 
embedded  in  the  substance  of  the  Amoeba.  For  example,  a  large 
Euglena  cyst  had  become  attached  to  the  hinder  end  of  an  Amoeba 
sphceronucleolus .  The  cyst  was  carried  upward  and  forward  on  the 
upper  surface,  and  at  the  same  time  it  began  to  sink  into  the  protoplasm, 
so  that  when  it  had  reached  the  anterior  edge  it  was  partially  embedded. 
It  was  then  rolled  under,  remained  at  rest  on  the  under  surface  in  the 
usual  way,  and  came  up  at  the  posterior  end.  It  was  now  deeply  sunk 
in  the  protoplasm,  yet  it  moved  forward  in  the  usual  way.  By  the 
time  it  had  reached  the  anterior  edge  again  it  no  longer  protruded 
above  the  surface  at  all.  After  turning  the  anterior  edge  again  it  sank 
completely  into  the  body,  still  surrounded  by  a  la3'er  of  ectosarc,  so 
that  it  passed  to  the  interior  of  the  Amoeba  as  a  food  Body.  I  have 
repeatedly  seen  bodies  which  were  thus  carried  forward  on  the  upper 
surface  gradually  taken  in  as  food.  They  always  continue  the  forward 
movement  even  when  completely  embedded  in  the  ectosarc.  It  is  thus 
evident  that  the  whole  thickness  of  the  ectosarc  partakes  of  the  forward 
movement.  The  forward  stream  in  ectosarc  and  endosarc  are  one  and 
continuous. 

The  relation  of  the  movements  of  the  outer  layer  to  the  lines  and 
wrinkles  seen  on  the  upper  surface  of  Amceba  verrucosa  and  its  rela- 
tives is  of  interest.  There  are  usually  two  sets  of  these  wrinkles,  one 
set  diverging  from  the  posterior  end  toward  the  direction  in  which  the 
animal  is  moving,  the  other  set  forming  a  number  of  curved  lines 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  I43 

parallel  to  the  advancing  edge  (Fig.  38).  These  wrinkles  and  the 
areas  which  they  enclose  do  not  change  markedly  as  the  Amoeba 
advances,  so  that  the  outer  surface  of  the  body  seems  to  be  quite  at 
rest.  It  is  this  fact,  I  believe,  that  has  prevented  the  true  nature  of 
the  movement  in  these  species  from  being  recognized  before.  Thus 
Penard  (1902,  p.  118),  after  a  thorough  study,  accurate  so  far  as  it 
goes,  of  the  movements  of  Amosba  verrucosa^  notes  that  many  facts 
point  to  the  existence  of  a  permanent  contractile  outer  layer,  but  holds 
that  the  permanence  of  certain  lines  and  patterns  on  the  upper  surface 
in  a  moving  Amoeba  is  crucial  against  the  idea  of  a  rolling  movement 
such  as  I  have  shown  above  to  actually  occur.  In  reality  these 
wrinkles  are  not  static  structures,  but  dynamic,  /.  e.^  the  substance  of 
which  they  are  formed  is  in  continual  motion  ;  they  are  like  the  per- 
manent ri'pples  on  the  surface  of  a  stream  where  the  latter  crosses  an 
obstruction.  The  wrinkles  indicate  the  direction  of  movement  of  the 
substance,  the  longitudinal  wrinkles  being  parallel  to  the  lines  of  motion, 
the  others  transverse  to  them.  A  particle  on  the  upper  surface  may 
move  parallel  with  the  longitudinal  wrinkles,  at  a  constant  distance 
from  them,  or  it  may  move  directly  along  one  of  these  wrinkles,  for 
the  whole  length  of  the  latter.  On  coming  to  one  of  the  transverse 
wrinkles  the  particle  moves  over  it  with  a  sort  of  jerk,  as  if  it  had 
passed  over  a  ridge  or  step,  as  indeed  it  has.  Thus  the  lines  and  the 
areas  enclosed  by  them  remain  constant,  while  the  substance  of  which 
they  are  composed  moves  onward. 

When  the  Amoeba  changes  in  a  marked  degree  its  direction  of 
movement,  so  as  to  follow,  for  example,  a  course  at  right  angles  to  the 
previous  one,  the  wrinkles  on  the  surface  usually  slowly  disappear,  then 
after  the  movement  has  become  well  established  in  the  new  direction, 
new  wrinkles  appear  in  correspondence  with  the  movement. 

When  such  a  change  of  course  occurs,  any  particles  on  the  upper 
surface,  which  were  moving  toward  the  anterior  edge,  change  their 
course  in  correspondence  with  the  new  direction  of  progression.  Fig. 
42  represents  a  case  of  this  kind,  where  an  Amoeba  verrucosa  bore  on 
its  upper  surface  a  minute  particle  of  debris  {a)  and  a  spherical  cyst  of 
Euglena  {b).  Both  moved  forward  over  the  stretch  x-y  (Fig.  42,  A), 
Now  a  little  methyl  green  {iri)  was  allowed  to  diffuse  against  the  left 
side  of  the  Amoeba.  The  animal  changed  its  course,  moving  to  the 
right  At  the  same  time  the  two  objects  a  and  b  changed  their  direction 
of  movement,  traversing  the  stretch  ^-^r  (Fig.  42,  B)  until  they  reached 
the  new  anterior  edge  of  the  Amoeba,  and  were  carried  underneath. 

The  free-moving  (upper)  surface  and  the  resting  (lower)  one  in 
contact  with  the  substratum  may  exchange  roles  at  any  time  when 
the  contact  with  the  substratum  is  changed.    Thus,  a  specimen  was 


144 


THE   BEHAVIOR   OF   LOWER   ORGANISMS. 


creeping  on  the  slide  and  bearing  on  its  upper  surface  a  small  granule, 
which  was  moving  forward  in  the  usual  way.  The  Amoeba  stopped 
and  raised  its  anterior  edge,  which  came  in  contact  with  the  cover 
glass ;  it  then  loosened  itself  entirely  from  the  slide,  while  its  upper 
surface  became  attached  to  the  cover.  It  now  began  to  move  forward 
on  the  cover  glass.  The  granule  on  the  upper  surface  now  remained 
quiet,  until  it  was  reached  by  the  posterior  end,  when  it  passed  down- 
ward to  the  lower  free  surface,  there  moving  forward  in  the  usual  way. 
Upper  and  lower  surfaces  had  completely  exchanged  roles.  In  a  sim- 
ilar way  I  have  seen  the  thin  lateral  edge  of  a  specimen  become  the 
middle  of  the  upper  moving  surface. 

Objects  of  the  most  varied  sort  cling  to  the  surface  of  Amoeba  verru- 
cosa and  its  relatives.  I  have  seen  the  following  attached  to  the  surface 
and  showing  the  typical  movements :  Particles  and  masses  of  soot, 
granules  of  India  ink,  motionless  bacteria,  diatom  shells,  dead  flagel- 
lates, masses  of  debris, 
cysts  of  Euglena,  a  small 
Amoeba  proteus  (the  lat- 
ter was  inclosed  after  it 
had  passed  to  the  under 
surface).  Usually  only 
one  or  two  small  objects 
are  seen  attached  to  any 
given  specimen,  but  to 
this  extent  the  phenomenon  is  very  common,  so  that  it  seems  rather 
surprising  that  the  movements  of  such  particles  should  not  have  been 
described  before. 

A  number  of  other  points  must  be  set  forth  before  we  can  form  a 
clear  conception  of  the  movements  of  these  Amoebae.  The  species 
under  consideration  are  much  flattened  and  have  usually  an  oval  form 
as  they  move  forward,  the  anterior-posterior  axis  being  the  longer, 
while  the  posterior  end  is  the  more  pointed  (Fig.  38).  Not  the  Whole 
lower  surface  is  in  contact  with  the  substratum,  but  only  a  band  at  the 
anterior  and  lateral  margins.     In  an  Amoeba  that  was  creeping  on  the 


Fig.  42.* 


*  Fig.  42. — Movement  of  bodies  attached  to  the  surface  in  Amoeba  verrucosa^ 
when  the  direction  of  locomotion  is  changed,  a,  A  small  granule ;  b,  a  Euglena 
cyst.  In  A  the  Amoeba  is  progressing  to  the  right,  as  shown  by  the  large  arrow ; 
the  two  bodies  attached  to  the  surface  moved  in  the  same  direction,  traversing 
the  stretch  x-y^  as  shown  by  the  small  arrows.  At  this  point  a  solution  of 
methyl  green  {vt)  was  allowed  to  diffuse  against  the  surface;  the  Amoeba  there- 
upon changed  its  course,  as  indicated  by  the  large  arrow  oi  B.  At  the  same 
time  the  bodies  a  and  b  changed  their  course,  traversing  the  stretch  y-z.  The 
stretch  x-y-z  in  B  shows  thus  the  path  of  the  attached  bodies  before  and  after 
the  reaction. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  1 45 

lower  surface  of  the  cover  glass  I  was  able  to  define  with  some  accuracy 
the  parts  that  were  attached  and  those  that  were  not.  A  small  flagel- 
late was  moving  briskly  about  between  the  Amoeba  and  the  cover  glass, 
but  its  excursions  were  limited  by  a  visible  line  running  parallel  with 
the  anterior  edge  of  the  Amoeba  and  extending  at  the  sides  back  to 
about  one-third  the  animal's  length  from  the  rear  (Fig.  43,  a-a-a) . 
The  zone  between  this  and  the  margin  was  pressed  close  to  the  glass, 
and  was  evidently  attached  to  it.  The  more  pointed  posterior  end  was 
held  quite  away  from  the  glass,  leaving  a  broad  passageway  through 
which  the  flagellate  finally  escaped. 

The  results  of  this  observation  were  confirmed  by  another.  An 
Amceba  verrucosa  in  full  career  was  suddenly  turned  on  one  lateral 
edge  by  a  strong  current  from  a  rotifer,  and  its  upper  edge  coming  in 
contact  with  the  cover  glass,  it  remained  in  that  position  some  time 
without  change  of  form.  It  could  be  seen  that  the  under  surface  was 
concave,  the  edges  very  thin  and  flat,  while  the 
posterior  portion  was  thick  and  arched  (Fig.  44). 

It  is  clearly  at  the  advancing  edge  of  the  ani- 
mal that  the  most  active  movements  are  taking 
place.  Here  the  hyaloplasm  may  be  seen  to 
push  forward  in  a  series  of  short  waves,  the 
anterior  edge  of  each  becoming  attached  to  the 
substratum.  At  the  same  time,  of  course,  an 
equivalent  amount  of  protoplasm  becomes  de- 
tached from  the  substratum  along  the  line  a~a-a^  ^  --^ss^?-^ 
Fig.  43,  though  this  does  not  take  place  in 
waves,  so  far  as  observable.  The  anterior  wave  must  in  some  way 
pull  upon  the  upper  surface  of  the  Amoeba,  bringing  it  forward,  and 
dragging  with  it  the  elevated  sac-like  posterior  end.  A  certain  feature 
of  the  advance  of  the  anterior  edge  seems  of  much  significance.  Each 
wave  seems  to  arise  just  behind  the  previous  anterior  boundary  line 
and  overlaps  it,  leaving  it  buried.  This  line  often  remains  visible  for 
a  short  time  after  the  new  wave  has  been  formed.  The  new  wave 
rolls  over  the  preceding  one  in  such  a  way  that  its  original  upper 
surface  becomes  applied  to  the  substratum.  This  is  demonstrated  by 
the  rolling  under  of  small  objects  on  the  upper  surface  of  the  advanc- 
ing wave.  A  diagram  of  the  movement  at  the  anterior  edge  is  given 
in  Fig.  45.  The  movement  can  be  imitated  roughly  by  making  a 
cylinder  of  cloth,  laying  it  flat  on  a  plane  surface,  and  pulling  forward 

♦  Fig.  43. — Attached  surface  oi Amoeba  verrucosa^  creeping  on  the  lower  surface 
of  the  cover  glass.  The  unshaded  portion  in  front  of  the  line  a-a-a  is  attached 
to  the  substratum,  while  the  shaded  portion  is  free  and  raised  slightly  above 
the  substratum. 


146  THK    BEHAVIOR    OF    I.OWER    ORGANISMS. 

the  anterior  edge  in  a  series  of  waves.     The  entire  cylinder  then  rolls 
forward  just  as  the  Amoeba  does. 

The  essential  features  of  the  movement  seem  to  be  (i)  the  advance  of 
the  wave  from  the  upper  surface  at  the  anterior  edge  ;  (2)  the  pull  exer- 
cised by  this  wave  on  the  remainder  of  the  upper  surface  of  the  body, 
bringing  it  forward.  Most  of  the  other  phenomena  follow  as  conse- 
quences of  these  two.  The  flowing  forward  of  the  granules  of  the 
endosarc  seems  to  demand  no  special  explanation,  since  a  fluid  con- 
taining granules  within  a  rolling  sac  must  necessarily  flow  forward  as 
the  sac  rolls.  By  the  movement  forward  of  the  anterior  end  a  space  is 
left  free  ;  by  the  rolling  forward  of  the  posterior  end  the  fluid  is  piled 
up  and  pressed  upon,  and  must  flow  forward  into  the  empty  space  in 
front.  Possibly  there  may  be  other  causes  at  work  in  producing  the 
endosarcal  currents,  but  such  currents  would  be  produced  without 
other  cause  in  a  sac  moving  as  Amoeba  does. 


3:4 

a        o 


Fig.  44.*  Fig.  45.! 


OTHER    SPECIES    OF    AMGBBA. 


Thus  far  we  have  dealt  only  with  Amoebae  of  rather  constant  form, 
which  do  not  produce  pseudopodia,  or  only  rarely  do  so.  We  must  now 
take  up  species  in  which  the  form  is  changeable  and  the  movements 
varied.  Of  such  species  I  have  studied  chiefly  Amoeba  limax^  A. 
proteus^  and  a  smaller  Amoeba,  which  I  take  to  be  Amoeba  angulata 
Meresch.  In  these  species  the  outer  surface  is  not  viscid,  except  at  the 
posterior  end,  so  that  small  objects  rarely  cling  to  it.  It  is,  therefore, 
much  more  difficult  to  determine  the  direction  of  movement  of  the 
upper  surface  than  in  Afjioeba  verrucosa  and  its  relatives.  Yet,  by 
mixing  soot  with  the  water,  and  devoting  a  sufficient  amount  of  time 
and  patience  to  the  work,  one  can  obtain  as  many  observations  as  he 
desires.     The  soot  settles  upon  the  upper  surface  in  particles  or  masses 


*FiG.  44. — Side  view  (partly  an  optical  section)  of  a  creeping  Amceba  verru- 
cosa, showing  the  thin  anterior  edge  {A)  attached  to  the  substratum,  and  the 
high  posterior  portion  (/*)  with  a  cavity  beneath  it. 

t  Fig.  45. — Diagram  of  the  movement  at  the  anterior  edge  of  Amceba  verrucosa. 
The  region  b-c  pushes  out,  taking  up  the  position  b'-c\  and  pulling  forward  the 
region  c-d,  so  that  it  comes  to  occupy  the  position  c'-d'.  The  point  a  remains 
in  its  place. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I47 

and  its  movements  can  be  followed  ;  at  times,  also,  objects  actually 
cling  to  the  surface,  as  in  the  other  species. 

The  results  are  essentially  the  same  as  in  the  species  already  described  ; 
foreign  particles  resting  upon  or  clinging  to  the  upper  surface  are  car- 
ried forward  to  the  anterior  edge.  Here  they  roll  over  the  edge,  passing 
beneath  the  Amceba,  which  now  moves  across  them.  As  a  rule  in 
these  species  particles  do  not  cling  to  the  surface  after  passing  to  the 
lower  side,  so  that  they  are  left  behind  when  the  posterior  end  passes 
over  them.  Sometimes  they  do  thus  cling,  however,  and  in  such  cases 
I  have  seen  them  pass  upward  at  the  posterior  end  and  again  forward, 
exactly  as  in  ^.  verrucosa  and  its  relatives.  In  order  that  my  state- 
ments may  not  remain  abstract  and  general,  I  copy  a  few  observations 
from  my  notebook,  all  relating  to  Amoeba  proteus. 

1 .  A  large  particle  of  debris  with  bits  of  soot  attached  to  it  was  seen 
lying  on  the  upper  surface  just  behind  the  middle.  It  was  carried 
forward  to  the  anterior  end  and  over  the  edge.  Then  it  came  to  rest 
on  the  bottom,  and  the  Amoeba  crept  over  it  till  it  was  passed  by  the 
posterior  end  and  left  behind. 

2.  A  number  of  soot  particles  on  the  upper  surface  just  in  front  of 
the  middle  were  carried  forward,  changing  their  direction  as  the  proto- 
plasmic currents  beneath  them  changed  direction.  They  were  finally 
carried  over  the  anterior  edge. 

3.  A  small  mass  of  soot  was  lying  on  the  middle  of  the  upper  surface. 
It  moved  forward  in  the  same  way  as  the  endosarcal  granules  under- 
neath. The  latter  changed  their  direction  of  movement  several  times  ; 
the  soot  mass  changed  correspondingly  at  the  same  time.  It  was 
finally  carried  over  the  anterior  edge,  where  it  could  be  seen  clearly 
separate  from  the  Amoeba. 

4.  A  large  mass  of  soot  one-quarter  the  size  of  the  Amoeba  was 
carried  forward  on  the  upper  surface  for  a  distance,  but  fell  off'  at  the 
side  before  reaching  the  anterior  end. 

5.  Two  small  masses  of  soot  lying  on  the  upper  surface  of  the 
posterior  end  were  carried  forward  over  the  anterior  edge. 

6.  Several  small  particles  were  clinging  to  the  lower  surface  of  the 
posterior  end.  They  passed  upward,  one  of  them  around  the  very 
middle  of  the  posterior  end,  to  the  upper  surface ;  here  they  were 
carried  forward  and  over  the  anterior  edge. 

I  could  add  a  large  number  of  such  observations. 

On  the  under  surface  the  particles  are  quiet,  as  I  have  shown  before 
(p.  136).  At  the  lateral  margins  the  edges  of  this  quiet  lower  surface 
are  seen,  so  that  particles  situated  here  are  usually  likewise  quiet,  until 
they  have  reached  the  posterior  part  of  the  Amoeba  (see  p.  135). 

As  to  the  details  of  the  movement  of  the  upper  surface,  the  following 


148  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

are  important.  Particles  situated  on  the  upper  surface  move  usually 
at  the  same,  or  nearly  the  same,  rate  as  the  granules  beneath  them,  in 
the  endosarc.  The  movement  of  the  surface  particles  follows  exactly 
that  of  the  endosarc  beneath  them,  changing  in  direction  when  the  latter 
changes.  Two  particles  close  together  on  the  upper  surface  may  thus 
diverge  or  even  flow  in  opposite  directions,  carried  by  two  different 
currents  which  are  visible  in  the  endosarc.  Any  portion  of  the  ecto- 
sarc,  like  any  portion  of  the  interior,  may  stop  at  any  time,  while  other 
parts  flow  onward.  One  may  thus  see  at  times  a  particle  at  rest  on  the 
upper  surface  of  a  moving  Amoeba.  Isolated  observations  of  this  kind 
might  lead  one  to  suppose  that  the  upper  surface,  like  the  lower,  remains 
at  rest  while  the  endosarc  passes  forward.  "But  when  a  particle  on  the 
surface  is  at  rest,  one  will  usually  find,  by  a  proper  change  of  focus, 
that  the  endosarc  beneath  it  is  likewise  at  rest.  It  is,  of  course,  well 
known  that  certain  portions  of  the  endosarc  may  be  at  rest  while  the 
remainder  is  in  movement  (see  Rhumbler,  1898,  p.  122).  In  the  same 
way  a  portion  of  the  outer  layer  may  sometimes  be  at  rest  while  the 
adjacent  endosarc  is  in  motion  ;  this,  however,  is  rather  unusual. 

We  may  sum  up  our  results  thus  far  in  the  following  statements  : 
In  an  advancing  Amoeba  substance  flows  forward  on  the  upper  sur- 
face^ rolls  over  at  the  anterior  edge^  coming  in  contact  with  the 
substratum^  then  remains  quiet  until  the  body  of  the  Amoeba  has 
passed  over  it.  It  then  moves  7ipward  at  the  posterior  end.,  and 
forward  again  on  the  upper  surface.,  continuing  in  rotation  as  long 
as  the  Amoeba  continues  to  progress.  The  motion  of  the  upper 
surface  is  congruent  with  that  of  the  endosarc^  the  two  forming  a 
single  stream. 

HISTORICAL,    ON    ROLLING    MOVEMENTS    IN    AMCEBA. 

The  possibility  that  Amceba  progresses  by  a  rolling  movement  was 
discussed  by  Claparede  &  Lachmann  (1858).  In  Amoeba  Umax  and 
Amoeba  quadrilineata  (=  A.  verrucosa) .,  according  to  these  authors, 
the  general  appearance  of  locomotion  is  in  many  respects  in  favor  of 
this  view  :  "  On  croit  positivement  voir  I'animal  rouler  sur  lui-meme  " 
(p.  435).  But  this  correct  view  is  rejected  (in  the  text)  because  of  the 
(supposed)  permanence  in  the  position  of  the  contractile  vacuole. 
Claparede  &  Lachmann  insist  that  the  contractile  vacuole  is  situated 
in  the  ectosarc  ;  hence,  they  argue,  if  there  were  a  rolling  movement 
of  the  ectosarc,  the  vacuole  would  necessarily  partake  of  the  movement ! 
In  a  note  on  p.  437  it  is  stated,  however,  that  Lachmann  personally 
believed  the  motion  to  be  of  this  rolling  character.  "  II  croit  s'etre 
assure  que  I' A.  quadrilineata  roule  sur  elle-meme."  According  to 
Claparede  &  Lachmann,  Perty  held  this  view  also. 


TtlE    AfOVEXfENTS    And    RHACtlONS    Oi^^    AMCEBA.  149 

Dr.  Wallich  shared  the  correct  opinion  of  Lachmann  and  Perty. 
This  excellent  observer  unfortunately  often  gave  his  results  in  the  form 
of  mere  brief  general  statements,  so  that  one  cannot  judge  how  much 
evidence  he  had  for  them,  and  little  attention  has,  therefore,  been  paid 
them.  But  it  is  singular  how  many  of  these  statements  show  them- 
selves to  be  correct,  even  in  opposition  to  later  work.  Concerning 
the  matter  in  question,  Wallich  has  the  following : 

In  short  the  effect  is  similar  to  that  which  would  be  produced  were  an  empty 
and  transparent  bladder  or  caoutchouc  sac,  containing  granular  bodies  of  greater 
specific  gravity  than  the  viscid  fluid  within  which  they  were  sustained,  to  be 
rolled  along  a  plain  surface.     (Wallich,  1863,  3,  p.  331.) 

He  makes  no  attempt  to  demonstrate  the  truth  of  this  correct  com- 
parison, and  does  not  develop  the  matter  beyond  the  mere  statement 
given  above. 

Schulze  (1875),  Berthold  (i8S6),  and  Butschli  (1892),  as  we  have 
seen,  agree  in  stating  that  the  currents  on  the  upper  surface  at  the 
anterior  end  in  Pelomyxa  are  backward.  In  view  of  the  great  authority 
of  these  writers  we  should  be  compelled  to  suppose  that  the  movement 
in  this  animal  is  of  an  entirely  different  character  from  that  found  in 
the  various  species  of  Amoeba,  but  for  a  most  fortunate  circumstance. 
The  only  previous  demonstrated  observation  of  the  forward  movement 
of  the  upper  surface  in  the  Rhizopoda  relates  precisely  to  Pelomyxa, 
and  was  made  by  an  investigator  closely  associated  with  Biitschli. 
It  was  not  until  my  work  was  finished  and  the  present  paper  written 
that  I  came  across  the  note  of  Blochmann  (1S94)  on  the  movements  of 
Pelomyxa.  Blochmann  shows  that  the  movement  of  substance  on  the 
upper  surface  of  Pelomyxa  is  forward,  just  as  we  have  found  it  to  be 
in  Amoeba.  The  outer  surface  of  Pelomyxa  is  covered  with  fine  cilia- 
like  projections.  By  observing  these  projections  Blochmann  had  no 
diflSculty  in  seeing  that  they  move  forward  on  the  upper  surface.  The 
rate  of  movement  was  the  same  as  that  of  the  internal  forward  current. 
Biitschli  (1892,  Appendix,  p.  220)  had  already  observed,  greatly  to  his 
surprise,  that  there  is  a  forward  current  in  the  water  next  to  the  sur- 
face of  an  advancing  Pelomyxa,  this  current  being  exactly  the  reverse 
of  that  called  for  by  the  theory  that  the  motion  is  due  to  a  lowering  of 
the  surface  tension  at  the  anterior  end. 

Biitschli  (/.  c.)  attempted  to  save  the  surface  tension  theory  by  sug- 
gesting that  it  was  only  a  thin  outer  layer  that  moves  forward.  The 
currents  in  the  moving  animal  would  then  be  as  follows :  A  forward 
current  within,  a  backward  current  just  beneath  the  surface,  a  forward 
current  in  a  thin  layer  on  the  surface.  It  is  possible  that  this  compli- 
cated arrangement  of  currents  might  be  brought  into  harmony  in  some 
way  with  the  surface-tension  theory  of  the   movement,  though  it  is 


150  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

rather  difficult  to  see  how  the  forward  movement  of  the  outer  layer 
would  be  produced.  As  we  have  seen,  Blochmann  found  that  the 
internal  and  external  forward  currents  move  at  the  same  rate  and  in 
the  same  direction.  It  is  difficult  to  explain  how  this  should  occur  if 
the  two  are  separated  by  a  layer  moving  in  the  opposite  direction. 
But  Blochmann  accepted  Biitschli's  suggestion,  and  attempted  to  give 
some  evidence  in  its  favor.  He  says  that  one  sees  the  outer  current, 
with  the  movement  of  the  projections,  in  places  where  the  marginal 
current  has  come  to  rest,  and  that  the  outer  and  internal  currents  then 
move  at  the  same  rate,  separated  by  the  resting  marginal  layer.  Now 
one  can  receive  exactly  this  impression  in  Amceba  in  the  following 
manner :  The  margins  where  they  are  pressed  against  the  substratum 
are  at  rest.  Just  above  this  region,  and  often  visible  in  the  same  focus, 
there  is  the  forward  current,  which  is  visible  on  the  one  hand  on  the 
surface  (through  the  movements  of  the  projections) ;  on  the  other  hand, 
in  the  interior  (through  the  movements  of  the  granules  of  the  endosarc). 
Unless  one  is  on  his  guard  as  to  the  slight  difference  in  level,  one  might 
seem  to  see  two  currents  separated  by  a  resting  layer,  particularly  if 
the  probability  that  this  were  true  had  been  suggested  beforehand.  It 
is  notable  that  Blochmann  describes  nowhere  outer  and  inner  forward 
currents,  separated  by  a  marginal  backward  current,  as  would  be 
required  by  the  modified  surface-tension  theory. 

We  have  demonstrated  above,  for  Amoeba  at  least,  that  the  forward 
movement  is  not  confined  to  a  thin  outer  layer,  but  extends  from  the 
outer  surface  to  the  endosarc  (p.  142) ;  in  other  words,  that  the  outer 
surface  moves  in  continuity  with  the  internal  substance. 

Rhumbler  (1898,  pp.  126-130)  discussed  at  length  the  possibility  of 
explaining  the  movement  of  Amoeba  by  means  of  a  rolling  sac  of 
ectoplasm,  only  to  come  to  the  conclusion  that  it  was  impossible. 
Rhumbler's  discussion  of  this  matter  is  an  excellent  example  of  the 
fact  that  acumen  and  excellent  reasoning  may  lead  one  astray  in  scien- 
tific matters  when  the  observational  basis  for  the  reasoning  is  not 
secure.  What  chiefly  misled  him  was  an  incorrect  idea  as  to  the 
direction  of  the  currents  in  the  substance  of  Amoeba,  particularly  his 
assumption  that  there  is  a  backward  current  on  the  upper  surface. 
The  diagram  which  he  gives  of  the  currents  as  they  must  occur  in  an 
Amoeba  moving  in  a  rolling  manner  (Fig.  33,  A,  p.  133)  is,  therefore, 
much  more  nearly  correct  than  that  in  which  he  shows  what  he  con- 
siders the  really  existing  currents  (Fig.  33,  B). 

Rhumbler's  conception  as  to  the  necessary  movements  in  the  sub- 
stance of  an  Amoeba  progressing  by  rotation  is,  however,  incorrect  in 
one  particular,  so  that  his  diagram  (Fig.  33,  A)  does  not  correspond 
to  the  facts  in  this  point.     He  assumes  that  there  must  be  a  backward 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  I5I 

current  on  the  lower  surface,  as  indicated  by  the  lower  (heavier)  arrows 
in  his  diagram  (Fig.  33,  A).  This  backward  current  does  not  exist, 
and  is  theoretically  unnecessary,  as  may  be  seen  by  making  a  cylinder 
of  cloth  and  moving  it  in  the  manner  described  above  (p.  145).  The 
under  surface  remains  at  rest  until  it  passes  upward  at  the  posterior 
end  {cf.  Fig.  40).  Rhumbler  held  that  this  backward  current  below, 
with  the  forward  current  above  (Fig.  33,  A)^  must  set  the  endosarc 
in  rotation  ;  "  the  endoplasma  granules  would  themselves  necessarily 
all  move,  like  the  particles  of  the  ectosarc,  in  circular  or  elliptical 
courses"  (p.  izS).  The  absence  of  such  circular  or  elliptical  paths  for 
the  granules  of  the  endosarc  would  then  speak  against  the  method  of 
movement  by  rotation  of  the  ectoplasm.  But  since  there  is  no  such 
backward  current  as  Rhumbler  assumes,  and  not  even  the  particles  of 
the  ectosarc  move  in  circular  or  elliptical  courses,  this  objection  falls 
to  the  ground. 

Further,  Rhumbler  seems  to  assume  that  for  locomotion  by  a  rotary 
movement  of  the  ectosarc,  the  latter  must  necessarily  be  a  "sharply 
defined  persistent  organ,"  and  that  its  contractions  could  only  be  due 
to  preformed,  permanent  fibers,  in  a  definite  arrangement.  Rhumbler 
is  able  to  show  of  course  that  these  two  assumptions  are  probably  incor- 
rect, and  considers  that  this  weighs  against  the  possibility  of  movement 
in  the  manner  characterized.  But  both  these  assumptions  are  unneces- 
sary. The  rotation  demonstrably  does  occur,  yet  the  permanent,  sharply 
defined  ectosarc  with  definitely  arranged  persistent  fibers  does  not  exist, 
as  Rhumbler  has  set  forth,  and  as  must  be  evident  to  anyone  who 
studies  for  a  long  time  the  changes  of  form  and  movement  in  Amoeba. 
As  we  shall  see  later,  a  simple  drop  of  fluid,  with  no  differentiated  outer 
layer,  may  move  in  the  same  manner. 

Penard  (1902)  also  discusses  the  possibility  of  movement  by  rotation 
of  the  ectosarc  in  Amoeba  verrucosa  (=  A.  terricold).  His  study  of 
the  movements  is  excellent  and  he  gives  as  a  possibility  on  p.  115  what 
is  really  in  its  main  features  a  nearly  accurate  statement  of  the  method 
in  which  locomotion  actually  occurs,  only  to  reject  this  possibility  later. 
The  ground  for  this  rejection  is  as  follows :  The  posterior  end  of  the 
Amoeba  often  bears  an  irregular  saclike  projection  (what  Penard  calls 
the  "  houppe"  )  ;  this  may  be  much  wrinkled  or  covered  with  projec- 
tions. This  wrinkled  sac  retains  its  position  ;  in  Amoeba  verrucosa  it 
is  covered,  like  the  rest  of  the  body,  with  a  resistant  cuticula,  which  can 
be  dissolved  only  with  great  difficulty  and  very  slowly. 

If  the  Amoeba  rolled  on  itself  in  progressing,  the  posterior  part  of  this  mem- 
brane would  necessarily  follow  the  movement  and  pass  little  by  little  forward, 
which  is  contrary  to  the  facts.  The  best  manner  of  assuring  one's  self  of  the 
immobility  of  the  pellicle  is  to  look  very  attentively  at  the  surfiice  of  the  con- 


152 


THE    BEHAVIOR    OF    LOVv'ER    ORGANISMS. 


tractile  vacuole;  there  one  sees  almost  always  very  fine  folds,  forming  angles 
and  varied  patterns;  these  angles  and  these  patterns  remain  for  a  long  time 
absolutely  the  same,  which  shows  that  nothing  has  changed  place.  (Penard, 
1902,  p.  118.) 

In  all  the  specimens  oi  Amoeba  verrucosa  and  A.  sphceronucleolus 
in  which  I  have  studied  the  matter,  the  posterior  part  of  the  outer  mem- 
brane does  follow  the  movement.  Particles  clinoring  to  the  outer  surface 
of  the  hinder  part  of  the  ectosarc  pass  upward  over  the  wrinkled  sac- 
like posterior  end  and  forward  on  the  upper  surface.  In  so  doing  they 
pass  directly  across  the  wrinkles  on  the  body  sur- 
face, as  set  forth  on  p.  143.  Had  Penard  chanced  to 
^      -    ^  see  the  movements  of  a  particle  attached  to  the  outer 

surface  of  the  body  he  could  not  have  been  misled 
by  the  apparent  permanence  of  the  surface  wrinkles . 

FORMATION  AND  RETRACTION  OF  PSEUDOPODIA. 

Thus  far  the  phenomena  in  Amoeba  proteus 
and  its  relatives  are  essentially  like  those  found 
in  Amoeba  verrucosa.  At  times  Atnoeba  proteus 
flows  forward  as  a  single  simple  mass  ;  then  its 
locomotion  may  be  compared  directly  in  its  chief 
features  to  that  of  A?nceba  verrucosa.  But  in 
Amoeba  .proteus  and  its  relatives  the  movement 
is,  of  course,  usually  much  complicated  by  the  for- 
mation of  pseudopodia.  In  considering  the  way 
in  which  these  are  formed  we  must  deal  separately 
with  two  different  cases,  depending  on  whether  the 
pseudopodium  when  sent  out  is  or  is  not  in  contact 
with  the  substratum. 

SURFACK  CURRENTS    IN   THE    FORMATION   OF  PSEUDOPODIA 
IN   CONTACT   WITH   THE    SUBSTRATUM. 

Fig.  46.*  When  the  pseudopodium  is  sent  out  in  contact 

with  the  substratum,  the  phenomena  accompany- 
ing its  formation  are  essentially  the  same  as  those  which  take  place  at 
the  anterior  end  of  an  advancing  Amoeba ;  the  latter  may  indeed  be 
considered  as  merely  a  large  pseudopodium.     Even  when  the  pseudo- 


♦FiG.  46.— Movement  of  a  particle  attached  to  the  outer  surface  of  a  pseudo- 
podium that  is  extending  in  contact  with  the  substratum.  At  a  the  particle  is 
at  the  middle  of  the  upper  surface;  at  b  it  has  nearly  reached  the  tip.  When 
the  pseudopodium  has  reached  the  length  shown  at  c  the  particle  has  passed 
over  its  tip.  Here  it  remains,  so  that  at  d,  when  the  pseudopodium  has  become 
longer,  the  particle  is  still  at  the  same  level,  but  on  the  under  surface  of  the 
pseudopodium,  some  distance  behind  the  tip. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


53 


podia  are  slender  and  pointed,  the  protoplasnn  flows  forward  (toward 
the  point)  on  the  free  upper  surface  and  in  the  interior,  while  on  the 
side  which  is  in  contact  with  the  substratum  the  protoplasm  is  at  rest. 
I  have  often  seen  small  particles  which  had  been  brought  forward  on 
the  surface  of  the  Amoeba  carried  out  to  the  tip  of  a  pseudopodium  on 
its  upper  surface,  finally  rolling  over  the  point  and  becoming  covered 
by  the  advancing  protoplasm  (Fig.  46). 

FORMATION    OF   FREE    PSEUDOPODIA. 

When  a  pseudopodium  is  sent  out  directly  into  the  water,  so  that  its 
surface  is  free  on  all  sides,  it  is  much  more  difficult  to  determine  the 
nature  of  the  movement.  Particles  rarely  cling  to  the  surface  of  such 
a  pseudopodium,  and  without  this  aid  one  cannot  be  certain  what  the 
movement  of  the  outer  layer  is.  However,  by  devoting  several  entire 
days  under  most  favorable  conditions  to  the  determination  of  this  point, 
I  collected  a  number  of  observations  which  demonstrate  clearly  the 
nature  of  the  move- 
ment. The  point  \  a  "b  ^ 
of  special  interest 
is,  here  as  else- 
whe  re  ,  whether 
there  is  a  back- 
ward current  on 
the  surface  of  the 
advancing  pseudo- 
podium, as  repre- 
sented  in   the  dia- 


FiG.  47.^ 


gram  from  Rhumbler,  Fig.  31.  To  this  the  observations  give  a  negative 
answer.  Particles  clinging  to  the  surface  of  a  pseudopodium,  whether 
at  the  tip  or  at  the  base  or  at  any  intermediate  point,  are  uniformly 
carried  outward,  in  the  same  direction  as  the  tip.  Particles  situated  at 
a  certain  distance  from  the  tip  of  a  short  pseudopodium  maintain  the 
same  distance  as  a  rule  when  the  pseudopodium  is  lengthened,  though 
in  so  doing  they  are  carried  far  out  from  the  body.  Sometimes  the  tip 
moves  outward  a  little  faster  than  the  parts  behind  it,  the  pseudopodium 
thus  becoming  more  slender  as  it  extends,  but  all  parts  agree  in  being 
carried  outward.  A  number  of  examples  of  actual  observations  will 
make  this  point  clear. 

I.  Amoeba  angulata  :  When  first  observed  there  was  a  short  pseudo- 
podium in  front,  projecting  freely  into  the  water.  A  small  particle  was 
attached  to  the  surface  at  about  the  middle  of  its  length  (Fig.  47,  a). 

*  Fig.  47. — Successive  stages  in  the  formation  of  a  free  pseudopodium,  showing 
the  movement  of  a  particle  attached  to  its  surface.  The  particle  moves  outward, 
keeping  at  approximately  the  same  distance  from  the  tip. 


154  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  pseudopodium  lengthened,  carrying  the  particle  with  it,  the  latter 
maintaining  its  distance  from  the  tip  nearly  or  quite  constant,  but  being 
carried  far  from  the  body  (Fig.  47,  b).  The  pseudopodium  finally  became 
very  long  and  slender  (c),  the  particle  remaining  attached  near  the  tip. 

2.  Amoeba  proteus :  A  particle  clinging  to  the  surface  of  one  side, 
near  the  anterior  end.  A  pseudopodium  was  formed  at  exactly  this 
point,  extending  freely  into  the  water,  so  that  the  particle  was  borne 
on  the  tip  of  the  pseudopodium.  It  maintained  this  position  while  the 
pseudopodium  was  extending,  and  was  still  found  at  the  tip  after  the 
pseudopodium  had  become  long  and  slender  (Fig.  48). 

The  third  example  which  I  give  is  one  of  much  interest,  because  it 
shows  the  movements  of  a  given  point  on  the  surface  in  both  the  retrac- 
tion and  extension  of  pseudopodia,  as  well  as  in  transference  from  the 
posterior  to  the  anterior  region  of  the  body. 

3.  Afnceba  proteus:    When  first  observed   the  animal   was   rather 

slender,  creeping  in  a  certain  direc- 
tion, and  with  two  long  pseudo- 
podia at  the  posterior  end,  extend- 
ing, one  on  each  side,  at  right 
angles  to  the  axis  of  progression 
(Fig.  49,  a).  The  left  pseudo- 
podium was  the  longer,  and  bore 
at  about  one-fourth  its  length  from 
its  base  a  small   particle   {x)   at- 

FiG.  48.*  tached    to    its    surface    by   a  very 

short  stalk  in  such  a  way  that  it 
was  seen  in  profile  (Fig.  49,  a).  The  pseudopodium  was  not  in 
contact  with  the  bottom,  and  was  slowly  retracting,  its  internal  con- 
tents flowing  into  the  body,  while  the  pseudopodium  itself  shortened. 
As  this  occurred  the  particle  approached  the  body  and  finally  passed 
on  to  its  surface  (<$,  c)  while  the  pseudopodium  was  yet  of  considerable 
length.  It  was  evident  that  the  shortening  of  the  pseudopodium  took 
place  chiefly  at  its  base,  since  the  part  between  the  base  and  the  particle 
X  had  become  incorporated  with  the  body  when  the  portion  between  a; 
and  the  tip  had  changed  only  a  little  in  length  (3,  c) .  This  distal 
portion  apparently  did  become  somewhat  shorter  at  the  same  time, 
while  its  surface  became  slightly  wrinkled.  By  the  time  the  tip  of  the 
pseudopodium  had  united  with  the  body  {d)  the  particle  x  had  moved 
a  considerable  distance  forward  on  the  latter.  The  posterior  portion 
of  the  body  was  here  thick,  and  the  particle  was  still  seen  in  profile, 
though  it  was  some  distance  above  the  substratum.     It  now  moved 


♦  Fig.  48. — Movement  of  a  particle  attached  to  surface  of  an  Amoeba  at  point 
where  a  free  pseudopodium  is  pushed  forth.     The  particle  remains  at  the  tip. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


155 


forward  very  slowly  (c,  d^  e)  till  at  f  it  passed  to  the  upper  surface. 
It  then  moved  rapidly  forward,  occupying  successively  the  positions 
indicated  by  the  line  of  circles  in  g.  (The  Amoeba  itself  was,  of  course, 
progressing  ;  no  attempt  is  made  in  the  diagram  to  represent  its  change 
of  position.)  Finally  the  particle  x  had  nearly  reached  the  anterior 
end,  when  the  latter  forked,  sending  two  pseudopodia  upward  and 
forward  into  the  water  (^,  h).  The  particle  x  was  at  first  at  the  base 
of  the  right  pseudopodium.  This  was  now  projected  forward  as  a  very 
long,  slender  pseudopodium  bearing  the  particle  x.  The  latter  was 
carried  steadily  out  from  the  body,  maintaining  almost  exactly  its 
original  distance  from  the  tip  of  the  pseudopodium  (Z^,  /, 7).     It  is 


Fig.  49.* 

possible  that  as  the  tip  became  very  slender  its  distance  from  x  became 
slightly  greater  as  if,  by  a  circular  contraction  of  the  intervening  part, 
the  tip  were  forced  further  out ;  but  there  was  no  movement  backward 
o{  x\  on  the  contrary,  it  moved  steadily  forward,  its  distance  from  the 
base  of  the  pseudopodium  continually  increasing.  Unfortunately  at 
this  point  the  animal  passed  under  a  mass  of  debris,  so  that  I  was 
unable  to  trace  further  the  history  of  that  point  on  the  body  surface 
marked  by  the  particle  x. 

I  have,  altogether,  about  a  dozen  observations  showing  this  outward 
movement  of  particles  on  the  surface  of  free  pseudopodia.     The  three 


♦  Fig  49. — Movements  of  a  particle  (a?)  attached  to  the  surface  of  Amoeba  in 
passing  from  a  pseudopodium  at  the  posterior  end  over  the  body  to  a  pseudopo- 
dium at  the  anterior  end.     For  explanation  see  text. 


156  TMK  Behavior  of  lower  orc^anIsMS. 

examples  above  given  are  typical  for  all.  They  show^  the  following  as 
to  the  manner  in  which  the  pseudopodia  are  formed  when  they  are 
projected  freely  into  the  water. 

1.  The  pseudopodium  grows  in  length  chiefly  from  the  base,  so  that 
any  part  on  the  surface  retains  nearly  its  original  distance  from  the  tip. 

2.  The  increase  in  surface  as  the  pseudopodium  grows  is  not  pro- 
duced by  the  flowing  outward  and  backward  of  the  endosarc  at  the  tip 
with  its  transformation  into  ectosarc  (as  represented  by  Fig.  31),  but 
by  the  transference  of  a  portion  of  the  surface  layer  of  the  body  to  the 
pseudopodium.  The  same  substance  remains  at  the  tip  of  the  pseu- 
dopodium from  the  beginning  (observation  2,  p.  154  ;  I  have  other 
observations  showing  the  same  thing). 

3.  Thus  the  movement  of  the  free  pseudopodium  is  like  that  of  the 
pseudopodium  in  contact  with  a  surface,  save  that  in  the  latter  case  one 
side  is  held  back  by  attachment  to  the  substratum.  In  the  free  pseudo- 
podium all  sides  move  outward  ;  in  the  attached  one,  all  sides  but  one. 

The  outer  layer  of  the  body  in  its  transference  to  the  pseudopodium 
may  doubtless  become  thicker  or  thinner  or  be  otherwise  modified.  As 
will  be  shown  later,  I  am  not  at  all  inclined  to  deny  the  possibility  of 
the  transformation  of  endosarc  into  ectosarc,  and  vice  versa.  The 
observations  show,  however,  that  this  transformation  of  substance  does 
not,  as  a  rule,  take  place  in  pseudopodia  by  means  of  the  ''fountain 
currents"  represented  in  the  diagrams  from  Rhumbler  (Figs.  30-32). 

Further,  the  surface  of  the  pseudopodium  may  be  increased  by  the 
flowing  into  it  of  the  endosarc,  producing  a  sort  of  stretching  of  the 
outer  layer,  involving,  of  course,  the  appearance  at  the  surface  of  por- 
tions of  substance  which  were  before  covered. 

WITHDRAWAL   OF   PSEUDOPODIA. 

In  the  withdrawal  of  pseudopodia  the  process  is  the  reverse  of  that 
occurring  in  the  formation  of  pseudopodia,  as  is  shown  in  case  3,  above 
(p.  154,  Fig.  49).  The  basal  parts  of  the  pseudopodial  surface  first 
pass  on  to  the  body,  followed  by  the  distal  portions. 

The  withdrawal  of  pseudopodia  shows  certain  other  features  that  are 
of  importance  for  the  understanding  of  the  mechanism  of  amceboid 
movement.  The  process  differs  somewhat  in  different  cases,  depending 
on  whether  the  withdrawal  is  slow  or  rapid.  When  the  pseudopodium  is 
slowly  withdrawn,  its  surface  may  remain  perfectly  smooth,  the  decrease 
in  surface  keeping  pace  with  the  decrease  in  volume,  until  the  pseudo- 
podium has  quite  disappeared.  But  when  the  withdrawal  is  more  rapid 
the  surface  becomes  thrown  into  folds  or  warty  prominences  of  various 
sorts.  This  is  more  common  than  retraction  without  the  formation  of 
such  prominences.      Evidently  the  volume  decreases  so  fast  that  the 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  I57 

decrease  in  surface  cannot  keep  pace  with  it^  so  that  the  surface  is 
thrown  into  folds.  This  phenomenon  is  particularly  interesting  in  its 
bearing  on  the  theory  that  would  account  for  the  retraction  of  pseudo- 
podia  by  the  action  of  surface  tension.  On  this  theory  we  should 
naturally  expect  the  surface  to  remain  smooth,  and  by  no  means  to  be 
thrown  into  folds,  since  it  is  by  the  tendency  of  the  surface  to  decrease 
that  the  decrease  in  volume  is  accounted  for ;  the  decrease  in  volume 
should  not,  therefore,  precede  the  decrease  in  surface.  This  matter  will 
be  taken  up  later. 

As  the  pseudopodium  decreases  in  size,  the  fluid  endosarc,  of  course, 
flows  out  of  it  and  joins  the  endosarc  of  the  body.  The  backward 
current  begins  at  the  mouth  or  inner  end  of  the  pseudopodium,  and 
gradually  extends  backward  to  near  the  tip  ;  the  current  is  most  rapid 
in  the  central  axis  of  the  pseudopodium,  and  in  this  axis  it  is  most 
rapid  at  the  inner  end.* 

Where  is  the  impelling  force  in  the  outflow  of  the  endosarc  and  the 
decrease  in  size  of  the  pseudopodium  ?  The  observations  seem  to  sug- 
gest several  factors  here.  The  fact  that  the  ectosarc  of  the  pseudo- 
podium passes  on  to  the  body  when  the  pseudopodium  shortens,  as  is 
shown  in  Fig.  49,  «,  b^  c,  indicates  that  the  ectosarc  of  the  body  exercises 
a  pull  on  the  outer  layer  of  the  pseudopodium,  drawing  it  inward. 
This  would,  of  course,  force  the  fluid  endosarc  into  the  body.  But  this 
would  not  account  for  the  wrinkling  and  roughening  of  the  outer  surface 
of  the  pseudopodium,  which  is  so  prominent  a  feature  in  the  withdrawal. 
For  this  there  are  two  conceivable  causes,  (i)  The  ectosarc  itself  may 
contract  actively,  driving  out  the  endosarc.  If  the  real  contractile  por- 
tion of  the  ectosarc  is  not  on  the  outer  surface  (in  the  cuticula,  as  it  has 
sometimes  been  called),  but  in  a  deeper  layer,  then  the  outer  surface 
would  be  thrown  into  folds  or  prominences  as  contraction  occurs.  (2)  On 
the  other  hand,  it  is  conceivable  that  the  endorsarc  might  be  drawn  out 
of  the  pseudopodium,  the  latter  collapsing  and  becoming  wrinkled  as 
a  result.  This  is  the  explanation  given  by  Biitschli  (1S92,  p.  201). 
This  view  would  have  to  assume  some  force  pulling  on  the  endosarc  at 
the  mouth  of  the  pseudopodium,  and  sufficient  viscosity  in  the  endosarc 
so  that  a  pull  thus  exercised  would  draw  out  the  whole  mass  contained 
within  the  pseudopodium.  Thus,  in  Fig.  49,  a,  the  general  advancing 
current  within  the  bod}^  of  the  Amoeba  might  be  thought  to  exercise  a 
pull  at  the  point  jK  in  the  direction  of  the  arrow ;  if  the  endosarc  were 


♦This  account  differs  from  that  given  b_y  Biitschli  (1880,  p.  116),  according  to 
whom  the  withdrawal  of  the  pseudopodium  begins  at  the  tip.  The  observations 
present  no  difficulty,  and  I  am  unable  to  understand  how  Biitschli  came  to  this 
result.  In  a  large  pseudopodium  the  method  of  retraction  described  above  is 
evident. 


158 


THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


sufficient!}'  viscous  the  entire  mass  of  endosarc  would  be  withdrawn, 
and  the  pseudopodium  would  collapse. 

There  are  certain  facts  that  speak  against  this  second  view.  Thus, 
the  endosarc  often  passes  out  when  there  is  no  current  away  from  the 
mouth  of  the  pseudopodium,  so  that  there  can  be  nothing  pulling  upon 
the  endosarc.  A  pseudopodium  may  be  withdrawn  when  the  animal 
is  otherwise  quiet ;  or,  when  the  animal  is  stimulated  strongly,  all  the 
pseudopodia  may  be  withdrawn  at  the  same  time,  while  there  is  no 
endosarcal  current  in  the  body  of  the  animal.  A  striking  case  that 
belongs  here  is  sometimes  to  be  observed  in  Amoeba  radiosa.  This 
animal  frequently  floats  in  the  water,  with  many  long,  pointed  pseudopo- 
dia radiating  in  all  directions  from  the  body.     Now,  if  the  pseudopodia 

are  stimulated  with  a  rod, 
they  begin  to  contract.  The 
endosarc  first  passes  inward, 
but  the  resistance  of  the  body 
is  so  great  that  the  fluid  stops 
at  the  base  of  the  pseudo- 
podia. These,  therefore, 
swell  up  in  a  bulbous 
fashion,  as  illustrated  in 
Fig.  50.  Such  cases,  indeed 
all  the  numerous  cases  in 
which  the  endosarc  passes 
out  of  a  pseudopodium  and 
comes  to  rest  as  soon  as  it  has 
left  the  latter,  can  only  be  ex- 
plained on  the  assumption 
that  the  endosarc  is  forced 
out  by  the  contraction  of  the  ectosarc,  or  by  some  active  movements  of 
the  endosarc  itself,  of  a  character  not  understood. 

Further,  there  are  certain  facts  which  speak  positively  in  favor  of 
the  view  that  the  production  of  the  wrinkles  is  due  to  a  contraction  of  the 
inner  layer  of  the  ectosarc.  Thus,  when  an  Amoeba  is  strongly  stimu- 
lated and  withdraws  all  its  pseudopodia  quickly,  the  whole  surface  of 
the  body  becomes  rough  and  wrinkled.  The  endosarc  has  not  passed 
out  of  it,  so  that  it  cannot  be  considered  in  a  state  of  collapse  ;  on  the  con- 
trary, it  is  clearly  contracted  as  strongly  as  possible.  Again,  if  a  large 
pseudopodium  is  cut  from  the  body,  it  contracts  strongly,  showing  the 
rough,  wrinkled  contour,  though  the  endosarc  has  not  passed  out  of  it. 


Fig.  50.* 


*FiG.  50. — Specimen  o{  Amoeba  radiosa  in  which  the  endosarc  has  passed  out 
of  the  distal  portions  of  the  pseudopodia  into  the  basal  parts,  causing  them  to 
swell  up  in  a  bulbous  fashion. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


159 


The  processes  occurring  in  a  retracting  pseudopodium  are  the  same 
as  those  taking  place  at  the  posterior  end  in  a  moving  animal.  In  fact, 
the  cases  are  really  identical ;  the  posterior  portion  of  the  body  may  be 
considered  merely  a  large  retracting  pseudopodium.  Often,  as  we  shall 
see,  it  is  impossible,  from  its  method  of  formation,  to  consider  it  any- 
thing else. 

The  pseudopodia  are,  of  course,  usually  formed  in  the  anterior  part 
of  the  Amoeba,  in  contact  with  the  substratum,  and  are  directed  in  the 
line  of  progression,  or 
at  a  slight  angle  with 
the  line  of  progression. 
As  they  are  withdrawn, 
their  surface,  as  we  have 
seen,  usually  becomes 
folded  or  roughened, 
and  the  small  roughened 
project  ion  resulting 
from  the  withdrawal 
lasts,  as  a  rule,  for  a  long 
time.  As  the  Amoeba 
continues  its  forward 
course,  the  base  of  the 
retracting  pseudopo- 
dium retains  nearly  its 
original  position,  as  do 
the  other  parts  of  that 
layer  of  the  ectosarc  that 
is  against  the  substra- 
tum, so  that  the  body 
of  the  Amoeba  gradually 
passes  the  pseudopo- 
dium, and  the  latter 
finally  becomes  united  with  the  posterior  end.  During  this  transference  to 
the  rear,  the  pseudopodium  usually  changes  its  position  (Fig.  51 ).  At 
first  it  is  directed  nearly  forward  (a) ,  then  it  takes  a  position  at  right 
angles  to  the  body  {^),  and  finally  swings  around  with  its  point  directed 


Fig.  5 


*  Fig.  51. — Successive  stages  in  the  retraction  of  a  pseudopodium.  At  a  the 
pseudopodium  extends  forward  at  the  anterior  edge  ;  at  3  it  has  partly  withdrawn 
and  stands  at  right  angles  to  the  body,  which  has  partly  passed  it;  at  c  the 
pseudopodium  is  directed  backward,  and  is  in  the  posterior  part  of  the  body;  at 
d  the  small  roughened  remnant  of  the  pseudopodium  has  nearly  united  with  the 
tail.  At  X  the  successive  positions  occupied  by  the  withdrawing  pseudopodium 
are  shown  in  a  single  diagram. 


l6o  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

nearly  backward  (Fig.  51,  c).  This  change  of  position  is  clue  to  the 
contraction  of  the  posterior  part  of  the  AmcEba.  The  ectosarc  just 
behind  the  base  of  the  pseudopodium  contracts  toward  the  middle,  as 
described  on  page  171.  As  a  result  the  pseudopodium  must  swing 
around  till  it  points  nearly  backward.  The  mechanism  of  the  process 
will  be  best  understood  by  an  examination  of  Fig.  51,  a*. 

Finally,  what  remains  of  the  pseudopodium  reaches  the  posterior 
end  or  tail  (Fig.  51,  d).  By  this  time  usually  all  that  is  left  of  it  is  a 
small  roughened  projection,  its  surface  being  of  essentially  the  same 
character  as  that  of  the  tail.  This  projection  fuses  completely  with  the 
tail,  its  projections  taking  up  a  portion  of  the  surface  of  the  latter.  The 
tail  is  in  fact  nothing  but  the  fused  remnants  of  all  the  pseudopodia 
that  have  been  formed,  together  with  the  contracted  outer  layer  of  the 
body  of  the  Amoeba  (the  latter  cannot  be  distinguished  in  any  essential 
way  from  a  pseudopodium).  A  roughened  tail  is  formed  de  novo  when- 
ever an  Amoeba  suddenly  changes  its  direction  of  movement.  The 
previous  anterior  end  then  becomes  roughened  in  contracting  and  forms 
a  typical  tail.  This  latter  unites  with  the  old  tail  if  any  of  the  latter 
remains.  The  substance  of  the  tail  gradually  passes  forward  into  the 
rest  of  the  body,  as  we  have  seen. 

MOVEMENTS    AT    THE    ANTERIOR    EDGE. 

As  in  Amoeba  verrucosa  and  its  relatives,  so  in  the  species  of  more 
changeable  form,  the  most  active  movements  are  taking  place  at  the 
anterior  edge.  In  Amceba  proteus  ?ind  A.  Umax  oxiq  sees  still  more 
distinctly  than  in  the  species  before  named  the  pushing  forward  of  a 
series  of  waves  of  hyaloplasm  which  become  attached  to  the  substratum 
in  front.  In  Amoeba  Umax  and  its  relatives  especially  such  a  wave 
may  be  very  pronounced,  extending  forward  at  times  one-fifth  the 
length  of  the  body  or  more,  though  usually  much  less. 

At  first  the  advancing  wave,  as  it  moves  rapidly  forward,  is  usually 
free  from  granules,  and  may  be  spoken  of,  therefore,  as  hyaloplasm. 
If  the  motion  is  less  rapid,  however,  it  contains  granules,  and  is  not 
distinguishable  in  any  way  from  the  interior  endosarc.  Where  it  is  at 
first  free  from  granules,  it  is  nevertheless  highly  fluid  in  character,  as 
is  shown  by  the  fact  that  it  flows  and  spreads  out  swiftly,  and  that  the 
granules  of  the  endosarc  pass  into  it  rapidly.  The  freedom  of  the 
advancing  hyaloplasm  from  granules  is  not  due  to  its  greater  density 
or  solidity  as  a  result  of  the  action  of  water  upon  it,  as  has  sometimes 
been  maintained,  for  it  is  at  first  free  from  granules  ;  then,  after  the 
water  has  acted  longer  upon  it,  it  becomes  filled.  Apparently  the 
reason  for  its  freedom  from  granules  is  merely  the  fact  that  it  moves 
forward  faster  than  the  granules  and  leaves  them  behind.     This  view 


THE    MOVEMENTS    AND    REACTIONS    OP'    AMCEBA.  IDI 

is  supported  by  the  variations  to  be  observed  in  the  relation  of  the  clear 
substance  to  the  granular  substance  at  the  anterior  end.  These  varia- 
tions arise  chiefly  from  the  different  rates  of  movement  of  the  two 
substances,  and  may  be  summarized  as  follows : 

I .  The  clear  substance  moves  fastest  at  first,  and  therefore  becomes 
separated  from  the  granules  as  a  broad  band  in  front  (Fig.  52,  a);  this 
is  then  immediately  filled  completely  by  the  granules.  Even  large 
granules  or  vacuoles  pass  to  the  very  anterior  edge,  so  that  one  sees 
but  a  line  between  these  and  the  outer  water. 


•i4-*--t;«:v'?:f>.»-»'-.o',     7/ 


Fig.  52.* 

2.  The  clear  substance  advances  fastest,  and  so  continues  to  do,  so  that 
it  remains  a  long  time  as  a  broad,  clear  band  in  front  of  the  granules. 

3.  The  two  substances  advance  at  the  same  rate,  so  that  there  is  no 
separation  between  them.    The  granules  and  vacuoles  are  then  found  at 


*  Fig.  52. — Distribution  of  hyaloplasm  and  granules  at  the  anterior  end  in 
Amceba  Umax  and  its  relatives  :  a,  hyaloplasm  without  granules  at  the  anterior 
end ;  b,  granules  and  vacuole  at  the  anterior  edge ;  c  and  d,  two  successive 
instants  in  the  locomotion ;  at  c  the  anterior  half  of  the  body  is  free  from  gran- 
ules, the  latter  being  heaped  up  behind  a  well-marked  barrier;  at  d  the  barrier 
has  burst  at  a  certain  point  {x),  allowing  a  stream  of  granules  to  flow  forward  to 
the  anterior  edge;  e  and/",  two  successive  stages  at  the  advancing  anterior  end; 
in  e  the  clear  hyaloplasm  has  stopped  at  the  line  x-y,  at/"  the  hyaloplasm  has 
advanced,  while  the  granules  are  heaped  up  behind  the  same  line  x-y. 


l62  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  advancing  edge.  This  condition  is  not  at  all  rare.  In  such  cases 
there  is  at  the  anterior  end  less  clear  space  between  the  granular  region 
and  the  water  than  in  any  other  part  of  the  body.  In  fact,  there  is 
typically  no  space  at  all.  I  have  seen  large  vacuoles  come  so  close  to 
the  anterior  edge  at  such  times  that  it  was  not  possible  to  distinguish 
between  the  boundary  of  the  vacuole  and  the  boundary  of  the  Amoeba 
(Fig.  52,  ^). 

4.  Finally,  either  hyaloplasm  or  endosarc  or  both  may  stop  in  any 
of  the  positions  mentioned  above.  Thus  the  hyaloplasm  may  stop, 
whereupon  the  endosarc  flows  into  it  and  fills  it,  or  both  may  stop,  so 
that  the  hyaloplasm  remains  empty,  as  a  clear  band,  for  a  long  time. 

The  line  separating  hyaloplasm  and  endosarc  is  at  times  very  sharply 
defined,  as  has  often  been  pointed  out.  A  number  of  unusually  favorable 
specimens  gave  me  the  opportunity  of  determining  the  reason  for  this, 
in  many  cases  at  least.  The  Amoeba  in  question  (Fig.  52,  c-f)  was  an 
elongated,  rapidly  moving  form,  much  resembling  A,  limax^  but  having 
usually  two  contractile  vacuoles,  one  very  large,  in  the  fore  part  of  the 
body,  the  other  smaller  and  in  the  rear.  The  body  contained  many 
fine  granules,  which,  when  the  animal  was  at  rest,  were  scattered  almost 
uniformly  through  the  body;  the  peripheral,  more  solid  zone  (usually 
called  ectosarc)  contained  as  many  of  these  as  did  the  endosarc. 

In  moving  this  Amoeba  usually  sends  out  first  a  large  amount  of  clear 
fluid  containing  no  granules  ;  this  at  times  extends  so  far  as  to  constitute 
half  the  length  of  the  Amoeba  (Fig.  52,  c).  There  is  a  perfectly  sharp 
line  between  the  clear  hyaloplasm  and  the  granular  endosarc,  and  behind 
this  line  the  granules  of  the  endosarc  are  heaped  up,  as  if  under  pressure. 
Suddenly  this  line  gives  way  over  a  small  area  (at  a*),  and  the  granules 
pour  through  it  in  a  thin  stream  nearly  or  quite  to  the  anterior  tip  of 
the  Amoeba  (Fig.  52,  d)*  Gradually  the  whole  barrier  gives  way,  and 
nothing  is  left  to  mark  the  position  it  occupied.  If  after  its  first  out- 
flow the  hyaloplasm  has  stopped,  the  whole  Amoeba  is  filled  with 
granules.  But  if,  as  is  usually  the  case,  after  a  pause  the  hyaloplasm 
has  started  forward  again,  the  granules  of  the  endosarc  stream  forward 
not  to  the  anterior  tip,  but  only  to  the  line  which  forfned  the  anterior 
boundary  of  the  hyaloplasm  at  its  pause  {x-y^  Fig.  52,  e^f).  Here 
the  granules  stop  and  are  heaped  up  again,  until  finally  the  barrier 
breaks  as  before,  and  the  granules  rush  forward  again,  to  be  stopped 
at  a  new  line. 

The  explanation  of  these  phenomena  becomes  evident  on  careful 
examination.  It  is  to  be  noted  that  the  line  x-y  which  stops  the 
flow  of  the  granules  of  endosarc  is  always  identical  with  one  which 


Similar  phenomena  have  been  observed  by  Prowazek  (1900,  p.  17;  Fig.  18). 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  163 

formed  the  anterior  boundary  of  the  hyaloplasm  (that  is,  of  the  Amoeba 
as  a  whole)  at  a  previous  pause.  The  reason  for  this  is  as  follows : 
The  lower  surface  of  the  Amoeba,  as  we  know,  is  at  rest ;  here  the 
protoplasm  has  become  modified  to  form  a  sort  of  membrane.  This 
membrane  extends  up  a  very  little  distance  at  the  sides  and  ends  (as 
is  shown  by  the  fact  that  the  protoplasm  at  the  sides  is  at  rest).  Thus 
at  the  anterior  end  there  is,  after  a  pause,  a  low  barrier  formed  by  this 
membrane.  The  next  wave  of  advancing  hyaloplasm  arises  just  behind 
this  barrier,  overleaps  it,  and  pushes  forward  (the  conditions  being 
essentially  the  same  as  in  Amoeba  verrucosa^  already  described).  This 
advancing  wave  when  first  formed  is  very  thin,  forming  a  mere  sheet 
lying  on  the  substratum.  This  is  shown  by  the  fact  that  when  the  out- 
line of  the  remainder  of  the  Amoeba  is  sharply  in  focus,  the  anterior 
portion  is  often  undefined,  and  one  is  compelled  to  focus  lower  to  get 
its  outline  sharply.  The  thin  sheet  of  hyaloplasm  which  has  just  pushed 
forward  is  bounded  behind  by  a  low  wall,  formed  from  the  membrane 
which  previouslylimit- 
ed  it  in  front  (Fig.  53, 
X).  Now  the  granules 
of  the  endosarc  flow  for- 
ward until  they  reach 
this  boundary ;  there 
they  stop  and  become 
heaped  up  against  it  (Fig.  53).  After  a  time  the  membrane  forming 
this  barrier,  since  it  is  now  completely  enveloped  by  protoplasm,  be- 
comes dissolved  and  gives  way  in  the  manner  described  above ;  the 
granules  then  flow  forward.  Meanwhile,  a  new  partial  boundary 
has  been  left  in  front  by  the  hyaloplasm  ;  this  again  stops  the  endosarc, 
and  the  whole  process  is  repeated  many  times. 

Of  course,  when  the  anterior  boundary  advances  uniformly,  without 
pauses,  no  anterior  membrane  is  formed,  and  there  is  nothing  to  hold 
back  the  granules  of  the  endosarc  ;  hence  there  is  no  reason  for  a  separa- 
tion of  hyaloplasm  and  endosarc,  and  we  find  that  none  exists.  On  the 
other  hand,  when  the  Amoeba  has  paused  for  a  long  time  the  anterior 

*  Fig.  53.— Diagram  of  a  longitudinal  section  of  the  anterior  edge  of  Amoeba, 
to  show  the  cause  of  the  stopping  of  the  granules  of  the  endosarc  some  distance 
behind  the  anterior  margin.  The  line  beneath  represents  the  substratum  to 
which  the  Amoeba  is  attached.  The  anterior  hyaloplasm  at  first  moves  forward  to 
the  line  x-x ;  stopping  there  it  becomes  covered  with  a  firmer  wall,  as  represented 
by  the  heavy  black  line.  Now  the  hyaloplasm  pushes  forward  from  above  the 
anterior  edge  x-x,  forming  a  thin  sheet  closely  applied  to  the  substratum,  as 
shown  in  the  figure.  The  endosarcal  granules  flow  forward,  but  are  stopped  by 
the  barrier  x-x  (the  former  anterior  boundary  of  the  Amoeba) ;  they  cannot  flow 
forward  till  this  boundary  is  liquefied. 


164  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

membrane  seems  especially  well  developed,  for  the  hyaloplasm  pushes 
then  a  long  way  ahead  and  may  form  half  the  length  of  the  Amceba 
before  the  endosarc  has  burst  through  the  membrane. 

The  phenomena  described  above  are  very  general  in  creeping  Amoebae, 
both  in  those  with  usually  but  a  single  pseudopodium  (as  A.  Umax), 
and  in  those  with  many  pseudopodia  (as  A.  angulata) . 

Of  course,  the  general  fact  that  there  is  a  separation  between  hyalo- 
plasm and  endosarc  is  not  explained  by  these  observations ;"  thus  we 
know  that  they  are  often  separated  even  in  pseudopodia  that  are  pro- 
jected freely  into  the  water.  But  the  phenomena  are  much  less  marked 
in  such  cases ;  it  is  exactly  the  observed  difference  between  them  and 
the  phenomena  to  be  seen  in  a  creeping  Amoeba  that  the  above  obser- 
vations explain. 

In  all  these  details  it  is  important  not  to  lose  sight  of  the  essential 
point  in  the  movement  at  the  anterior  end.  This  is  as  follows  :  The  new 
wave  begins  on  the  upper  surface  just  behind  the  former  boundary  line, 
and  rolls  forward,  so  that  its  former  upper  surface  is  now  in  contact 
with  the  substratum.  * 

This  method  of  movement  explains  a  peculiar  fact  which  one  observes 
frequently,  and  which  I  found  it  difficult  to  understand  before  this 
movement  was  demonstrated.  The  advancing  edge  in  Amoeba  usually 
does  not  push  forward  fine,  loose  particles  lying  on  the  substraturti  in 
front  of  it,  but  overlaps  them  instead,  so  that  the  Amoeba  creeps  over 
them.  This  is  especially  noticeable  when  the  water  contains  many 
particles  of  India  ink  or  of  soot.  In  view  of  the  rolling  movement  with 
the  series  of  waves,  each  coming  from  behind  the  previous  anterior 
edge  and  thus  descending  on  the  substratum  from  above,  this  burying 
of  loose  movable  particles  becomes  intelligible. 

In  Amoeba  proteus  and  its  relatives  the  advancing  anterior  edge  does 
not  move  forward  in  a  single  uniform  curve,  as  it  does  in  A.  verru- 
cosa, and,  as  a  rule,  in  A.  Umax,  On  the  contrary,  the  anterior  edge 
may  show  the  most  varied  form  and  modeling  (Fig.  54)  ;  narrow  points 
may  be  sent  out  here  ;  a  broad  rounded  lobe  there  ;  a  rectangular  projec- 
tion elsewhere.  Pseudopodia  may  rise  above  the  general  level,  pro- 
jecting freely  into  the  water  and  later  coming  in  contact  with  the 
substratum,  or  be  withdrawn  without  Coming  thus  in  contact.  The 
anterior  portion  of  the  body  may  divide  into  two  lobes,  or  may  become 
hollowed  out  so  as  to  contain  a  cavity  bounded  by  thin  walls  (see 
later,  Figs.  75,  76).  These  facts  show  clearly  that  the  method  of 
advance  of  the  anterior  edge  cannot  possibly  be  determined  by  general 
pressure  from  behind,  such  as  would  be  produced,  for  example,  by  a 
contraction  of  the  posterior  part  of  the  body.  Such  pressure  could  not 
produce  the  cavity  shown  in  Fig.  75  or  the  thin  edge  bearing  numerous 
points  shown  in  Fig.  54. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


65 


MOVEMENTS    OF    THE    POSTERIOR    PART    OF    THE    BODY. 

In  an  Amoeba  moving  as  a  simple,  elongated  mass,  the  anterior  por- 
tion of  the  body  is  broadest  and  very  thin,  being  flattened  against  the 
substratum,  while  the  posterior  part  is  narrower  and  much  thicker.  In 
many  cases  the  posterior  end  rises  to  an  actual  hump,  the  body  being 
thickest  at  the  posterior  edge,  or  a  little  in  front  of  this  edge  (Figs.  44, 
58).  This  is  true  as  well  of  the  Amoebse  of  nearly  constant  form  (A. 
verrucosa,  etc..  Fig.  44),  as  of 
those  related  to  A.  proteus.  From 
this  hump  the  upper  surface  slopes 
forward  to  the  thin  anterior  edge. 
The  margins  in  the  posterior  part  of 
the  body  are  not  thin,  but  rounded 
like  the  surface  of  a  cylinder. 

The  anterior  portion  of  the 
Amoeba  is  attached  to  the  substra- 
tum. This  attachment  of  the  ante- 
rior portion  has  been  clearly  demon- 
strated by  Rhumbler  (1898),  and  I 
can  confirm  his  results  throughout. t 
The  attachment  is  probably  by  a 
mucus-like  secretion  ;  at  least  such 
a  secretion  exists,  as  Rhumbler  and 

others  have  shown  and  I  can  confirm.  I  have  sometimes  been  able  to 
pull  an  Amoeba  about  by  using  a  glass  rod  to  which  a  thread  of  this 
mucus  had  become  attached  (Fig.  55).  The  animal  then  seems  to 
follow^  the  rod  at  a  distance,  the  thread  of  mucus  not  being  visible. 
In  virtue  of  this  attachment  the  Amoeba  resists  currents  of  water, 
or  the  impinging  of  solid  bodies  against  it.  The  posterior  portion 
of  the  body  is  not  thus  attached,  but  is  entirely  free  from  the  bottom. 

In  many  cases  the  most  posterior  part  of  the  body  forms  a  more  or 
less  distinctly  marked  off  portion,  the  surface  of  which  is  wrinkled  or 
warty  or  villous,  or  otherwise  irregular.  This  is  variously  known  as 
the  tail,  the  villous  patch,  or  appendage  (Wallich,  Leidy),  houppe 
(Penard),  Schopf  (Rhumbler),  etc.  The  occurrence  of  this  appendage 
is  variable.  In  some  species  it  is  usually  present,  in  others  less  com- 
mon. Its  occurrence  and  degree  of  development  vary,  indeed,  in  the 
same  individual. 


Fig.  54.^ 


♦Fig.  54. — Amosba  angulata  in  locomotion,  showing  the  numerous  points  in 
the  anterior  region,  some  attached  to  the  substratum,  others  projecting  freely  into 
the  water,     a  is  the  "antenna-like"  pseudopodium,  described  on  p.  177. 

tit  is  rather  curious  that  Butschli  (1892),  in  his  discussion  of  the  movements 
of  Amoeba,  is  inclined  to  deny  that  there  is  any  attachment  to  the  substratum. 


l66  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

In  an  advancing  Amoeba  the  posterior  end  moves  forward  at  about 
the  same  rate  as  does  the  anterior,  since  the  distance  between  the  two 
remains  about  the  same.  Leaving  out  of  account  for  the  moment 
specimens  with  the  wrinkled  appendage,  there  is  a  continual  current 
forward  from  the  posterior  end.  Nevertheless,  the  latter  remains  on 
the  average  of  about  the  same  size.     The  material  which  flows  out  of 

it  above  is  supplied  from 
beneath.  As  we  have 
seen,  a  layer  of  material 
at  the  under  surface  of 
the  Amoeba  is  at  rest. 
The  main  portion  of  the 
body  passes  over  this 
layer,  dragging  the  pos- 
^^^'  ^^*  terior  end.     The   latter 

takes  up  as  it  passes  the  resting  layer  which  was  against  the 
substratum.  This  gradually  becomes  fluid,  and  passes  for- 
ward again  in  the  advancing  current.  All  this  may  be 
clearly  seen  by  observing  the  course  of  individual  particles 
in  the  protoplasm  and  on  the  surface,  and  is  fully  set 
forth  in  the  preceding  pages  of  this  paper. 

The  unattached  posterior  portion  steadily  contracts  as  it 
moves  forward.  Particles  on  its  upper  surface  are  moving  forward,  as 
we  have  seen  in  detail.  But  this  is  not  all.  Particles  on  its  sides  and 
under  surface  likewise  move  forward ;  there  is  an  actual  contraction 
independent  of  the  streaming  already  described.  The  movement  of 
substance  due  to  this  contraction  is  more  striking  and  rapid  as  we 
approach  the  posterior  end.  As  this  contraction  is  an  important  fact, 
it  will  be  well  to  give  some  details  of  the  observations  which  show  it 
to  exist. 

Particles  attached  to  the  lower  surface,  or  to  the  lateral  margins  of 
the  Amoeba,  next  to  the  substratum,  in  the  anterior  part  of  the  body, 
remain  quiet  for  a  long  time.  But  this  lasts  only  till  they  have  reached 
that  portion  of  the  body  which  is  free  from  the  substratum  ;  then  they 
begin  to  move  slowly  forward  as  a  result  of  the  contraction  just 
described.  Of  two  such  objects,  one  nearer  the  posterior  end,  the 
hinder  one  moves  the  more  rapidly,  so  that  the  distance  between  the 
two  slowly  but  distinctly  decreases.  Though  such  objects  on  the  bot- 
tom or  sides  move  forward,  they  do  so  less  rapidly  than  does  the 
posterior  end.  The  latter,  therefore,  in  time  overtakes  them,  and  they 
are  finally  pulled  around  the  posterior  end  to  the  upper  surface,  where 
they  pass  forward,  as  we  have  already  seen  in  detail. 

♦  Fig.  55. — An  Amoeba  drawn  backward  by  a  thread  of  its  viscid  secretion. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


167 


Fig.  56. 


The  contraction  of  the  posterior  part  of  the  body  is  further  shown  by 
the  behavior  of  retracted  pseudopodia.  When  a  pseudopodium  con- 
tracts it  usually  produces,  as  we  have  seen,  a 
small  wart-like  excrescence,  which  persists 
for  some  time.  Such  wart-like  remains  of 
pseudopodia  behave  like  foreign  bodies  at- 
tached to  the  margin  of  the  Amoeba.  In  the 
anterior  half  they  remain  quiet,  while  in  the 
free  posterior  half  they  move  slowly  forward, 
as  a  result  of  the  contraction  of  this  part  of 
the  body.  When  two  or  more  of  these  rem- 
nants of  pseudopodia  are  formed  at  once, 
with  an  interval  between  them,  this  interval 
becomes  less  as  a  result  of  the  more  rapid 
movement  of  the  hinder  one. 

The  contraction  of  this  posterior  region  is 
sometimes  very  striking,  especially  when  the 
posterior  end  becomes  attached  to  some  for- 
eign object  and  is  drawn  out  longer  than 
usual ;  when  it  finally  becomes  free  it  con- 
tracts suddenly  and  rapidly.  Thus,  for  example,  an  Amoeba  hav- 
ing the  form  shown  in  Fig.  56,  a,  began  to  move  in  the  direction 
shown  by  the  arrow,  when  it  became  evident  that  the  posterior  end  was 
attached  to  a  diatom  shell,  which  was  fast  to  the  substratum.  As  the 
Amoeba  crept  away  the  posterior  end  was  drawn  out,  as  shown  at  6. 
Finally  the  diatom  became  detached  from  the  bottom,  when  the  stretched 
posterior  end  at  once  contracted,  shortening  up  rapidly,  so  that  the 
Amoeba  had  the  form  shown  at  c.     Such  observations  are  often  made. 

This  contraction  does  not  occur  in  that  part  of  the  Amoeba  which  is 
attached  to  the  bottom,  but  begins  at  once  as  soon  as  the  attachment 
ceases.  One  might  compare  the  outer  layer  to  a  stretched  sheet  of  India 
rubber  that  is  attached  to  a  surface  by  means  of  some  adhesive  sub- 
stance. As  soon  as  the  adhesion  gives  way  the  sheet  contracts.  There 
is  no  definite  point  at  which  the  attachment  to  the  substratum  must 
cease  ;  sometimes  it  is  farther  forward,  sometimes  farther  back.  The 
gradual  freeing  of  the  posterior  portion  can  be  clearly  observed  in  many 
cases,  particularly  in  Amoeba  angulata^  and  may  be  seen  to  go  hand 
in  hand  with  the  contraction  of  the  ectosarc.  As  soon  as  a  certain  part 
of  the  body  becomes  free,  its  contraction  takes  place  with  some  sudden- 
ness, and  the  contraction  is  the  more  noticeable  the  greater  the  part  of 
the  body  that  is  freed  at  once.     Often  the  process  of  becoming  freed 

*  Fig.  56. — Successive  forms  of  an  Amoeba,  showing  the  marked  contraction 
of  the  posterior  end.     (See  text). 


1 68  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

takes  place  in  a  series  of  jerks,  and  there  is  a  corresponding  jerkiness 
in  the  contractions  of  the  posterior  part  of  the  body.  When  a  large 
amount  of  surface  is  freed  at  once  there  is  a  sudden  forward  rush  of  the 
fluid  portion  of  the  Amoeba,  with  a  striking  contraction  of  the  posterior 
part  of  the  body.  Such  a  case  as  is  shown  in  Fig.  56  is  only  an  unusu- 
ally strong  contraction  of  this  sort,  due  to  the  fact  that  the  hinder  part 
on  the  body  had  remained  locally  attached  longer  than  usual. 

As  a  result  of  this  contraction,  the  ectosarc  of  the  posterior  part  of 
the  body  becomes  thickened  and  wrinkled,  or  warty.  The  change  from 
a  flat  plate  to  a  rounded  form  involves  a  decrease  in  the  amount  of  exter- 
nal surface,  and  as  the  amount  of  material  in  the  surface  layer  is  not  at 
once  decreased,  this  layer  is  compelled  to  fold  and  become  wrinkled  and 
warty.  When  this  process  is  very  pronounced  we  have  produced  at 
the  posterior  end  the  wrinkled,  warty  appendage  so  often  described. 
Such  a  roughened  structure  may  be  produced  in  any  part  of  the  AmcEba 
by  rapid  contraction,  as  we  have  seen  above  (p.  160).  The  rough, 
warty  appendage  at  the  posterior  end  is  the  common  product  of  all  the 
contractions  which  have  taken  place. 

In  Amoeba  verrucosa  and  its  relatives  the  current  forward  on  the  upper 
surface  extends  backward  to  the  posterior  end  ;  the  outer  surface  of  the 
latter  seems  not  markedly  different  in  texture  from  that  of  the  rest  of 
the  body.  In  other  species  of  Amoeba  there  is  a  greater  difference 
between  the  texture  of  the  surface  layer  of  the  anterior  part  of  the  body 
and  that  of  the  posterior  end,  and  this  may  involve  some  differences  in 
the  movements.  Often,  in  even  these  species,  the  forward  current 
extends  backward  to  the  very  posterior  end  ;  particles  on  the  under  side 
pass  up  over  the  posterior  end  and  forward,  just  as  in  A.  verrucosa 
(see  p.  147).  But  in  other  cases,  in  A.  limax^  A.  froteus^  etc.,  the 
surface  material  at  the  posterior  end  is  so  stiffened  that  it  is  temporarily 
excluded  from  the  current.  There  is  then  produced  the  distinct,  rough- 
ened appendage,  which  is  for  a  time  dragged  passively  behind  the 
Amoeba.  In  such  a  case  the  currents  from  beneath  pass  upward  on 
either  side  of  this  appendage,  meeting  in  the  middle  line  (Fig.  57). 
Particles  attached  to  the  under  surface  on  either  side  of  the  appendage, 
therefore,  soon  pass  to  the  upper  surface  and  are  carried  forward,  while 
those  on  the  under  surface  of  the  appendage  itself  may  remain  in  position 
and  be  dragged  forward  for  a  considerable  time. 

But  I  have  rarely  found  this  posterior  appendage  so  completely  cut 
off'from  the  general  circulation  as  is  often  supposed.  Usually  there  is 
a  very  slow  current  forward  on  the  upper  surface  of  the  appendage, 
involving  also  its  internal  parts.  Into  this  current  particles  attached 
to  the  posterior  end,  and  even  to  the  under  surface  of  the  appendage, 
are  in  course  of  time  drawn.    I  have  thus  seen  particles  of  soot  dragged 


THE    MOVEMENTS   AND    REACTIONS    OF   AMCEBA.  1 69 

about  for  ten  minutes  at  the  posterior  end,  then  finally  pass  upward  into 
the  surface  current,  where  they  were  carried  to  the  anterior  end.  Even 
when  this  slow  current  from  the  posterior  appendage  is  completely 
suspended  the  suspension  is  only  temporary.  The  currents  after  a  period 
begin  again,  and  a  strongly  marked  warty  posterior  appendage  may  in 
time  completely  disappear,  its  substance  hav- 
ing become  mingled  with  that  of  the  remain- 
der of  the  Amoeba. 

Other  parts  of  the  Amoeba  may  become 
temporarily  immobile  and  thus  excluded  from 
the  general  circulation.    One  often  sees  certain  Fig.  57.* 

parts  of  Amoeba  proteus  and  other  similar  species  thus  quiet,  while  the 
restof  thebody  is  in  active  motion  (see  Rhumbler,  1S9S,  p.  122). 

In  the  species  with  ^-eruptive"  pseudo  podia  this  process  seems  to 
have  gone  farthest.  Here  the  whole  outer  layer  apparently  becomes 
hardened  at  times,  so  that  movement  occurs  only  when  the  inner  sub- 
stance bursts  through  this,  forming  "eruptive"  pseudopodia.  In  this 
case  the  pseudopodia  formation  apparently  differs  from  that  in  A?noeba 
proteus  and  its  relatives,  as  described  above,  in  the  fact  that  the  ectosarc 
of  thebody  is  not  transferred  to  the  surface  of  the  pseudopodium.  I 
have  not  been  able  to  study  this  process  in  detail  further  than  to  deter- 
mine that  there  is  no  backward  current  on  such  pseudopodia.  The 
matter  is  worthy  of  further  examination.  In  Amoeba  verrucosa^  the 
species  which  has  been  hitherto  supposed  to  have  the  most  immobile 
ectosarc,  we  have  shown  that  the  outer  layer  is  in  continual  rotary 
motion  in  the  progressing  animal. 

GENERAL  VIEW  OF  THE  MOVEMENTS  OF  AMCEBA  IN  LOCOMOTION. 

Let  us  now,  with  the  aid  of  a  diagram,  attempt  to  form  a  clear  con- 
ception of  the  movements  occurring  in  an  Amoeba  that  is  progressing 
in  a  definite  direction,  with*  a  view  to  determining  the  nature  of  the 
forces  at  work.  Fig.  58  may  represent  a  longitudinal  section  of  such 
an  Amoeba  as  seen  in  a  side  view.  The  anterior  end,  A^  is,  as  we  have 
seen,  very  thin,  and  is  applied  closely  to  the  substratum,  while  the 
posterior  end,  /*,  is  high  and  rounded,  forming  a  sort  of  pouch.  It  is 
free  from  the  substratum,  beginning  at  the  point  a*,  at  about  the  middle 
of  the  body. 

At  the  anterior  end  waves  of  hyaloplasm  are  pushed  forward  one 
after  the  other,  so  that  the  anterior  end  successively  occupies  the  posi- 
tions a,  3,  c.  As  we  know,  it  is  the  upper  surface  which  thus  pushes 
out ;  it  rolls  over,  so  that  a  point  which  was  originally  on  the  upper 

*FiG.  57. — Diagram  of  the  surface  currents  when  the  posterior  appendage  ic 
excluded  from  the  general  stream. 


lyO  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

surface  becomes  applied  to  the  substratum.  It  is  evident  that  the  sur- 
face of  the  Amoeba  is  increased  in  extent  by  the  pushing  out  of  these 
waves. 

On  the  upper  surface  of  the  Amoeba  there  is  a  forward  current  of  the 
outer  layer,  as  indicated  by  the  arrows.  This  current  extends  back- 
ward to  the  posterior  end,  where  it  is  continued  as  a  movement  upward 
from  the  lower  surface.  This  upward  movement  stops,  at  any  given 
movement,  at  about  the  point  _y,  though,  of  course,  the  point  where 
it  ceases  cannot  be  precisely  fixed.  That  part  of  the  lower  surface 
which  is  in  contact  with  the  substratum,  from  the  anterior  end  to  x^  is 
quiet.  That  part  of  the  lower  surface  which  is  not  in  contact  with  the 
substratum  (from  x  io  y)  is  moving  slightly  forward  owing  to  the  con- 
traction in  this  region,  as  described  on  pages  166-168.  This  movement 
is  comparatively  slight,  as  indicated  by  the  small  arrows.     Within  the 


Fig.  58.* 

Amoeba  are  currents  moving  forward  in  the  same  direction  as  the 
current  on  the  upper  surface. 

The  posterior  end  as  a  whole  moves  forward,  so  that  it  comes  to 
occupy  later  the  position  shown  by  the  dotted  line.  The  point  x^ 
where  the  lower  surface  of  the  Amoeba  becomes  free  from  the  sub- 
stratum, moves  forward  an  equivalent  amount  to  x.  The  entire 
Amoeba  thus  moves  forward  in  the  direction  indicated  by  the  large 
arrow  above. 

Thus  far  our  account  has  been  purely  descriptive,  containing  only 
what  has  been  demonstrated  by  observation  and  experiment,  and  intro- 
ducing nothing  hypothetical.  We  must  now  endeavor  to  form  a  con- 
ception of  the  location  and  direction  of  action  of  the  forces  at  work  in 
producing  the  movements.  Discussion  of  the  ultimate  character  of 
the  forces  will  be  reserved  for  the  section  on  the  theories  of  amoeboid 
movement. 

One  of  the  primary  phenomena  is  evidently  the  pushing  forward  of 

*  Fig.  58.— Diagram  of  the  movements  of  Amoeba,  as  seen  in  side  view.  A^ 
anterior  end;  P,  posterior  end;  a,  b,  c,  successive  positions  occupied  by  the  an- 
terior edge.  The  large  arrow  above  shows  the  direction  of  locomotion;  the 
other  arrows  show  the  direction  of  the  protoplasmic  currents,  the  longer  arrows 
indicating  the  more  rapid  currents.     For  further  explanation  see  text. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I7I 

the  anterior  edge.  The  form  of  the  Amoeba  shows  that  this  cannot  be 
due  to  pressure  from  behind,  for  if  the  pressure  were  greatest  behind 
and  less  in  front,  the  mass  of  internal  fluid  would,  of  course,  be  forced 
forward,  and  the  Amoeba  would  be  thickest  in  front  instead  of  behind ; 
the  form  of  anterior  and  posterior  ends  would  be  reversed.  In  the 
varied  modeling  of  the  anterior  end  we  have  seen  another  proof  of  the 
impossibility  of  accounting  for  the  action  here  by  pressure  from  behind 
(p.  164).  Further,  the  forward  current  on  the  upper  surface  of  the 
Amoeba  could  not  possibly  be  produced  by  pressure  from  behind. 
The  impossibility  of  accounting  for  the  form  and  movement  by  pres- 
sure from  behind  has  been  recognized  by  most  investigators,  though 
on  other  grounds  than  those  here  set  forth. 

On  the  other  hand,  if  we  take  the  view  that  the  anterior  wave,  after 
attaching  itself  to  the  substratum,  exercises  a  pull  on  the  parts  behind 
it,  the  rest  of  the  phenomena  follow  most  naturally.  Such  a  pull 
would  draw  forward  the  tenacious  upper  layer  of  the  body,  and  we 
find  that  this  is  actually  moving  forward.  The  mass  of  inactive  inter- 
nal contents  would  drag  behind  as  far  as  possible,  so  that  the  thickest 
part  of  the  Amceba  would  be  at  the  rear,  and  this  is  exactly  what  we 
find  to  be  true.  The  posterior  end  would  be  dragged  forward.  This, 
also,  is  true.  In  its  movement  forward  it  would  be  partly  rolled  ;  that 
is,  its  lower  surface  would  gradually  pass  upward  and  become  the  upper 
surface.  This,  also,  we  know  to  be  true.*  Finally,  the  internal  fluid 
contents  would  be  compelled  to  stream  forward  as  the  anterior  end 
advanced  and  the  posterior  end  followed  it.  This  streaming  is,  of 
course,  one  of  the  striking  features  of  the  Amoeba.  The  character- 
istics of  the  endosarcal  streaming  are,  I  believe,  exactly  what  might 
be  expected  from  the  method  of  origin  just  set  forth. 

We  have  one  other  more  or  less  independent  factor  of  the  movement 
in  the  contraction  of  the  posterior  part  of  the  body  that  is  not  in  con- 
tact with  the  substratum.  As  we  have  seen,  the  substance  of  the  sides 
and  bottom,  as  well  as  of  the  upper  surface,  are  moving  forward  in 
this  region,  as  indicated  by  the  small  arrows  of  the  diagram  (between 
^and^).  Moreover,  we  know  that  there  is  a  lateral  contraction  as 
well  as  an  antero-posterior  one,  for  the  wide,  flat  anterior  portion 
shrinks  together  as  soon  as  it  is  released  from  the  substratum.  This 
contraction  should  probably  be  brought  into  relation  with  the  previous 
increase  of  surface  at  the  anterior  end.  As  the  anterior  wave  is  sent 
forth  the  surface  at  the  anterior  end  is  much  increased.  We  might  com- 
pare the  action  with  the  stretching  of  a  sheet  of  India  rubber.  This 
tense  portion  then  becomes  attached  to  the  substratum,  as  we  might 

*  Large  bodies  within  the  Amoeba  close  against  the  posterior  surface  are  often 
rolled  over  in  this  process,  as  I  have  several  times  observed. 


172  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

fasten  the  stretched  sheet  of  India  rubber  by  means  of  a  strong  cement 
to  a  plate  of  glass.  Upon  being  released  the  tense  layer  of  protoplasm 
contracts  again,  just  as  the  rubber  sheet  would  do.  In  the  protoplasm 
the  contraction  takes  place  rather  slowly,  causing  the  steady  pulling 
forward  of  the  posterior  half  of  the  body,  as  exhibited  by  objects  attached 
to  its  lower  surface. 

In  connection  with  the  contraction  of  the  lower  surface  as  just  de- 
scribed we  must  consider  also  certain  properties  of  the  upper  surface. 
When  this  is  pulled  upon  by  the  advancing  anterior  wave  it  does  not 
respond  like  an  inelastic  membrane,  but  like  an  elastic,  contractile  one. 
If  it  were  inelastic  its  motion  would  follow  that  of  the  anterior  end 
exactly,  and  thus  take  place  in  a  series  of  jerks.  But  this  does  not 
occur.  When  the  anterior  wave* pushes  forward,  thus  extending  the 
upper  surface,  there  is  no  immediate  increase  in  the  movement  of  this 
surface,  nor  of  the  posterior  end  ;  the  movement  forward  is  a  steady 
one.  The  property  of  contractility  is  further  shown  very  directly  in  the 
phenomena  which  take  place  when  a  large  portion  of  the  lower  surface 
of  the  Amoeba  is  suddenly  released,  as  described  on  page  167.  It  seems 
clear  that  the  entire  surface  of  the  Amoeba  is  in  a  state  of  tension  and  that 
this  tension  is  directed  toward  the  advancing  anterior  end.  The  condi- 
tion would  be  imitated  by  partly  filling  a  rubber  sack  with  a  heavy  fluid, 
causing  one  surface  to  adhere  to  the  substratum  and  pulling  on  one  side. 

As  a  result  of  this  tension  on  the  surface  the  internal  contents  of  the 
Amoeba  must,  of  course,  be  under  a  certain  slight  amount  of  pressure. 
As  we  have  seen  (p.  171)  even  without  this  pressure  the  internal  con- 
tents must  flow  forward,  since  the  posterior  surface,  against  which 
they  are  resting,  is  moved  forward.  But  the  pressure  accounts  for 
certain  details  of  the  movements  of  the  endosarc.  Thus,  when  a  pseudo- 
podium  is  sent  forth,  or  one  of  the  anterior  waves  moves  forward,  it  is 
usually  soon  filled  by  endosarc.  In  its  pushing  forward  the  pseudo- 
podium  forms  a  region  where  the  tension  is  relieved  ;  the  fluid  contents, 
under  pressure  elsewhere,  therefore  flow  into  it. 

It  is  to  be  noted  that  this  pressure  is  a  mere  consequence  of  the  tension 
due  to  the  pushing  forward  of  the  anterior  edge,  and  is  by  no  means  a 
cause  of  the  pushing  forward  ;  it  is  always,  therefore,  subordinate  to  and 
dependent  upon  the  latter,  and  is  not  a  matter  of  primary  significance. 

Altogether,  then,  our  results  lead  us  to  look  upon  Amoeba  as  an  elastic 
and  contractile  sac,  containing  fluid.  In  locomotion  one  side  of  this  sac 
actively  stretches  out,  becomes  attached  to  the  substratum,  and  draws 
the  remainder  of  the  sac  after  it  in  a  rolling  movement.  The  primary 
phenomena  are  the  stretching  out  of  one  side,  the  elasticity,  and  the 
contractility  of  the  outer  layer. 

Whether  this  elasticity  and  contractility  should  not  be  considered 


THE    MOVEMENTS   AND    REACTIONS    OF    AMOEBA.  1 73 

properties,  not  merely  of  the  outer  layer,  but  of  the  entire  substance  of 
the  Amoeba,  may  be  a  question.  The  fact  that  ectosarc  and  endosarc 
are  mutually  interconvertible  would  seem  to  imply  an  affirmative  answ^er 
to  this  question,  and  I  believe  other  evidence  could  be  adduced  looking 
in  the  same  direction.  But  the  locomotion  itself  seems  to  require  these 
properties  only  in  the  ectosarc,  so  that  we  shall  for  the  present  leave  out 
of  consideration  the  question  as  to  their  existence  in  the  endosarc. 

To  the  three  primary  phenomena  above  mentioned  we  must  devote 
further  attention.  It  has  been  maintained  by  certain  writers  that  the 
ectosarc  is  not  an  elastic  and  contractile  membrane,  as  above  set  forth  ; 
hence  we  must  examine  the  evidence  on  that  point.  There  then  remain 
the  questions  :  What  is  the  cause  of  the  pushing  out  at  the  anterior  edge  ? 
and.  What  is  the  essential  nature  of  the  contractility  of  the  ectosarc  .!* 
These  questions  will  be  reserved  for  a  special  section  on  the  theories 
of  amoeboid  movement.  We  will  at  this  point  investigate  certain 
general  properties  of  the  substance  of  Amceba,  with  a  view  espe- 
cially to  determining  whether  we  are  justified  in  considering  the 
ectosarc  elastic  and  contractile,  though  not  limiting  our  attention  to 
these  properties  alone. 

SOME  CHARACTERISTICS  OF  THE  SUBSTANCE  OF  AMCEBA. 
FLUIDITY. 

It  is,  of  course,  not  necessary  to  dwell  upon  this  point ;  it  has  been 
treated  in  detail  recently  by  Rhumbler  (189S,  1902)  and  Jensen  (1900). 
For  anyone  who  is  familiar  with  the  movements  of  Amoeba  from  per- 
sonal observation,  doubt  cannot  exist  that  its  protoplasm  has  at  least 
some  of  the  most  striking  properties  of  fluids,  notably  the  property  of 
flowing,  with  the  freedom  of  movement  of  the  particles  with  reference  to 
each  other  that  this  implies.  This  applies  most  strongly  to  the  endosarc  ; 
for  the  ectosarc,  as  we  shall  see,  there  are  decided  limitations  to  the 
fluidity.  Nevertheless,  the  particles  of  the  ectosarc  have,  to  a  considera- 
ble degree,  that  freedom  of  movement  with  relation  to  each  other  that  is 
characteristic  of  fluids.  This  is  shown,  for  example,  by  the  fact  that  any 
portion  of  the  ectosarc  may  be  temporarily  excluded  from  the  advanc- 
ing stream  (especially  common  at  the  posterior  end,  p.  169),  and  in  the 
fact  that  neighboring  portions  of  the  ectosarc  may  flow  in  opposite 
directions  (p.  148) .  But  the  characteristics  of  the  ectosarc  are  much 
more  those  of  a  tough,  rather  persistent  skin  than  has  sometimes  been 
supposed.     This  point  is  brought  out  in  the  following  sections. 

rhumblkr's  "  knto-ectoplasm  process." 
The  movements  of  the  outer  layer  of  the  body  described  in  this  paper 
have  an  important  bearing  on  the  transformation  of  endosarc  into  ecto- 
sarc and  vice  versa^  of  which  so  much  is  said  in  Rhumbler's  recent 


1^4  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

extensive  paper  (1898).  My  observations  show  that  this  transforma- 
tion is  confined  within  much  narrower  limits  than  Rhumbler  supposed. 
In  the  account  which  he  gives  of  the  movements  of  Amoeba  this  trans- 
formation (the  "  ento-ectoplasm  process,"  as  he  calls  it)  plays  a  very 
large  part,  and  is  essential  to  locomotion.  At  the  anterior  end,  accord- 
ing to  Rhumbler,  endosarc  constantly  flows  out  to  the  surface  and  is 
there  transformed  into  ectosarc,  flowing  back  as  such  along  the  surface 
of  the  body.  Somewhere  in  the  posterior  part  of  the  body  or  at  the  base 
of  a  pseudopodium  this  ectosarc  passes  inward  and  is  retransformed 
into  endosarc.  These  supposed  processes  are  indicated  in  the  diagrams 
from  Rhumbler,  Figs.  30-33. 

My  observations  show  that  this  view  of  the  constant  inter-transforma- 
tion of  the  two  layers  is  incorrect,  and  that  we  must  attribute  to  the 
ectosarc  a  much  higher  degree  of  permanence  than  Rhumbler  supposed. 
There  is  no  regular  transformation  of  endosarc  into  ectosarc  at  the 
anterior  end.  On  the  contrary,  the  ectosarc  here  retains  its  continuity 
unbroken,  moving  across  the  anterior  end  in  the  same  manner  as  across 
other  parts  of  the  body.  In  the  same  way,  the  ectosarc  is  not  regularly 
transformed  into  endosarc  in  the  hinder  part  of  the  body.  We  can  trace 
a  single  definite  point  on  the  ectosarc  (or  a  complex  of  such  points 
having  a  definite  relation  to  each  other)  continually  until  it  has  passed 
completely  around  the  Amoeba  ;  several  complete  rotations  of  this  sort 
are  described  from  actual  observation  on  page  141 .  In  the  species  having 
very  changeable  forms  a  single  point  on  the  ectosarc  may  be  traced, 
for  example,  from  the  surface  of  a  pseudopodium  at  the  posterior  end 
across  the  whole  length  of  the  body  to  near  the  tip  of  a  long  pseudo- 
podium at  the  anterior  end  (Fig.  49,  p.  155) ;  there  is  no  reason  to 
suppose  that  it  could  not  be  traced  indefinitely  but  for  the  difficulties 
of  observation. 

On  the  other  hand,  there  is  no  doubt  that  ectosarc  may  be  trans- 
formed into  endosarc,  and  vice  versa,  under  certain  conditions.  This 
process  was  apparently  first  clearly  seen  by  Wallich  (1863,  a,  p.  370). 
Wallich  saw  the  formation  of  "  eruptive  pseudopodia  "  by  the  outflow 
of  the  endosarc  through  a  small  perforation  in  the  ectosarc.  A  portion 
of  the  latter  was  thus  covered  by  the  endosarc,  and  gradually  resorbed. 
Rhumbler  figures  a  similar  case  (1S9S,  p.  152),  and  I  have  repeatedly 
seen  such.  Further,  as  Rhumbler  has  shown,  and  as  I  can  confirm,  in 
A.  verrucosa  food  bodies  are  enclosed  in  a  layer  of  thick  ectosarc,  which 
passes  with  the  food  into  the  endosarc,  there  to  be  resorbed  (seep.  195). 

Thus,  it  is  clear  that  there  may  be  a  transformation  of  one  layer  into 
the  other  under  special  circumstances,  but  such  transformation  is  much 
less  general  than  Rhumbler  supposed,  and  is  by  no  means  a  regular 
accompaniment  of  locomotion. 


THE    MOVEMENTS   AND    REACTIONS    OF   AMCEBA. 


^1S 


ELASTICITY   OF   FORM   IN   AMCEBA. 

For  a  real  understanding  of  the  phenomena  shown  by  amoeboid 
protoplasm  it  is  important  to  realize  that  it  has,  besides  some  of  the 
chief  characteristics  of  fluids,  a  number  of  properties  that  are  usually 
considered  characteristic  of  solids.  This  came  out  clearly  in  certain 
of  my  experiments.  They  show  that  Amoeba  has  elasticity  of  form  to 
a  considerable  degree. 

These  experiments  consisted  in  changing  the  shapes  of  Amoebae  with 
a  fine  capillary  glass  rod,  under  the  microscope,  in  the  open  drop. 
From  numerous  experiments  of  this  character  the  following  may  be 
selected  as  typical : 

An  Amoeba  had  sent  out  one  rather  long,  thick  pseudopodium,  as 
shown  in  Fig.  59,  a.  With  the  capillary  glass  rod  this  pseudopodium, 
«,  was  pulled  loose  from  the  bottom  and  bent  over  into  the  position 
shown  by  the  dotted  outline  b.     On  being  released  it  rather  quickly 

a 


c  f 


Fig.  59.* 


Fig.  6o.t 


sprang  back  into  its  original  position,  a.  This  experiment  was  repeated 
on  different  Amoebae  many  times. 

An  elongated  Amoeba  {a-a^  Fig.  60)  was  bent  with  the  rod  at  about 
its  middle,  so  that  the  anterior  half  was  pushed  far  to  one  side  of  the 
original  median  axis  (to  b) .  This  anterior  half  at  once  attached  itself 
to  the  bottom,  whereupon  the  posterior  half,  which  was  not  attached, 
immediately  swung  round  into  line  with  it,  so  that  the  Amoeba  occu- 
pied the  position  b-c.  Thus  the  original  straight  Amoeba  on  being 
bent  immediately  straightens  itself  out  again.  On  repeating  this  experi- 
ment with  many  elongated  individuals  it  was  found  that  frequently  the 
straightening  out  was  not  quite  complete,  so  that  after  it  had  occurred 
there  was  still  a  slight  bend  in  the  middle. 

An  Amoeba  had  a  long  pseudopodium  curved  over  to  one  side,  as  in 
Fig.  61,  a.     This  pseudopodium  was  loosened  from  the  bottom  with 


♦Fig.  59. — A  straight  pseudopodium,  a,  is  bent  into  the  position  b  with  a  rod. 
It  at  once  returns  to  the  position  a. 

tFiG.  60. — A  narrow  Amoeba,  a-a,  is  bent  with  the  rod  into  the  position  a-b  , 
the  end,  b,  then  becomes  attached,  and  the  animal  at  once  straightens  into  the 
position  b-c. 


176  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

the  rod  and  straightened  out  (6).     On  being  released  it  at  once  swung 
back  to  its  original  form  and  position  at  a. 

An  Amoeba  had  many  long,  slender,  free  pseudopodia  standing  out 
radially  from  the  body.  These  could  be  pushed  repeatedly  to  one  side 
or  the  other,  or  bent  at  a  marked  angle.  In  every  case  they  returned 
at  once  to  the  radial  position. 

An  indefinite  number  of  such  experiments  could  be  detailed.     They 

show  clearly  that  Amoeba  has,  to  a  certain  degree  at  least,  one  of  the 

most  distinctive  properties  of  solids,  a  tendency  to  resist  deformation  of 

shape,  and  to  restore  the  shape  when  changed.     It  will  be  observed 

that  the  cases  are  not  such  as  can  be  accounted  for  on  the  assumption 

that  Amoeba  is  a  simple  fluid  mass  which  tends  to  take  a  certain  form 

in  accordance  with  the  principle  of  least  surfaces.     A  small  sphere  of 

fluid  when  deformed  returns  to  its  original  shape  in  conformity  with 

the  principle  just  mentioned.     But  such  returns  to  the  original  form  as 

^~,^  ^  are  illustrated  in  Fig.  59 

(       \  and  Fig.  61,  for  example, 

y^     ^     """""""^--v.     \       \  are   not  required    by  the 

(]^  1        \  principle  of  least  surfaces 

^\^  V.^ X -' "^^  ,  so  long  as  the  Amoeba  is 

^v^....^^^  )  J  ^  considered  a  simple  fluid 

— -"^^  mass. 

^^'''  ^'■*  On  the  other  hand,  if 

we  consider  Amoeba  not  as  a  simple  fluid,  but  as  a  fluid  mass  of 
a  foamlike  or  alveolar  structure,  composed  of  a  tense  meshwork  of  one 
fluid  enclosing  minute  drops  of  another,  then  the  results  above  set 
forth  might  be  explained  without  assuming  that  the  protoplasm  has 
in  any  part  passed  from  a  liquid  to  a  solid  state.  This  follows 
from  the  considerations  and  experiments  recently  set  forth  by  Rlium- 
bler  in  a  most  important  and  suggestive  paper  (1902).  Rhumbler 
shows  that  a  fluid  mass  having  alveolar  structure  must  react  to  tran- 
sient pressure  from  without  like  an  elastic  body  ;  in  other  words, 
that  it  must  have  elasticity  of  form.  The  results  which  I  have  set 
forth  above  might  almost  seem,  then,  to  have  been  predicted  in  Rhum- 
bler's  summing  up:  "Transient  tensions  or  pressures  produce  an 
elastic  reaction  of  the  cell  body;  longer  action,  on  the  other  hand, 
produces  a  plastic  reaction  "  (/.  c,  p.  371).  For  the  detailed  demonstra- 
tion of  this  principle  the  reader  must  be  referred  to  the  original  paper 
of  Rhumbler.  It  will  suffice  to  note  here  that  the  result  is  due  to  the 
fact  that  deformations  of  the  body  as  a  whole  produce  deformations  of 
the  alveoli,  and  that  the  surface  tension  of  the  alveolar  walls  tends  to 

♦  Fig.  61. — A  large,  curved  pseudopodium,  a,  is  straightened  out  into  the  posi- 
tion d  with  a  rod.     On  being  released  it  at  once  returns  to  the  position  a. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  1 77 

restore  them  at  once  to  their  original  form,  resulting  in  a  return  of  the 
whole  body  to  its  original  form. 

If,  then,  we  hold  that  the  substance  of  Amoeba  is  composed  of  such 
an  alveolar  structure,  the  above  observations  are  intelligible,  even 
though  no  part  of  the  substance  of  the  organism  is  in  the  solid  state. 
But  whatever  the  cause,  we  must  recognize  that  the  protoplasm  of 
Amoeba  shows  in  the  gross  some  of  the  characteristics  .of  solids. 

Leaving  out  of  account  the  minute  structure  of  the  protoplasm,  most 
or  all  of  the  observations  detailed  above  could  be  accounted  for  on  the 
assumption  that  the  body  of  Amoeba  consists  of  a  sac  of  fluid,  the  outer 
wall  of  the  sac  being  tough  and  elastic,  and,  as  is  shown  later,  contrac- 
tile. In  this  case  only  the  outer  layer,  the  ectosarc,  would  show  the 
characteristics  of  matter  in  the  solid  state  of  aggregation.  Certain 
observations  made  by  the  writer  indicate  that  this  is  the  true  state  of  the 
case.  These  observations  are  as  follows  :  In  several  cases  a  long,  slender 
pseudopodium,  formed  of  both  endosarc  and  ectosarc,  was  stimulated  at 
the  tip,  causing  the  endosarc  to  be  withdrawn,  and  leaving  the  pseudo- 
podium formed  of  ectosarc  alone,  as  illustrated  in  Fig.  50,  page  158.  Such 
pseudopodia  could  with  the  glass  rod  be  bent  sharply  at  an  angle,  and 
would  often  remain  thus  for  some  time.  If,  while  thus  sharply  bent, 
the  endosarc,  as  sometimes  happens,  begins  to  flow  back  into  the 
pseudopodium,  the  latter  straightens  out  with  a  sort  of  jerk  as  soon  as 
the  endosarc  begins  to  fill  it.  The  ectosarc  thus  acts  like  an  empty 
glove-finger,  which  might  bend  over  when  empty  but  which  would 
straighten  out  on  becoming  filled  with  a  fluid.  A  tough  skin  could 
perhaps  be  formed  by  an  alveolar  fluid  in  accordance  with  the  princi- 
ples developed  by  Rhumbler  as  above  set  forth.  Whatever  the  explana- 
tion, the  experiments  indicate  the  existence  of  this  tough  skin-like  layer 
on  the  outer  surface  of  the  body. 

CONTRACTILITY    IN   THE   ECTOSARC   OF   AMCEBA. 

Besides  elasticity  of  form,  the  outer  layer  of  Amoeba  clearly  has  the 
power  of  contracting  locally.  This  is  a  fact  which  is  omitted  from 
consideration  in  many  of  the  theories  in  which  amoeboid  movement  is 
referred  to  local  changes  in  the  surface  tension  of  a  fluid  mass.  It  will 
be  well,  therefore,  to  set  forth  some  of  the  observations  on  this  point. 
I  transcribe  here  some  of  my  notes,  with  the  corresponding  sketches. 

1.  Specimen  with  a  single  long,  prominent,  curved  pseudopodium. 
This  rather  quickly  swings  around  bodily  toward  its  concave  side,  and 
unites  with  the  protoplasm  of  the  body  (Fig.  62,  a). 

2.  A  specimen  sends  out  a  long,  curved  pseudopodium  (Fig.  62,  6). 
This  slowly  straightens  out,  passing  from  position  i  to  position  2. 

3.  A.  angulata  usually  sends  out  at  the  anterior  end  a  single 
pointed  pseudopodium  obliquely  upward  into  the  water  (Fig.  62,  c). 
This  point  frequently  waves  from  side  to  side  like  an  antenna. 


178 


THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


4.  An  Amoeba  was  creeping  on  the  surface  film,  with  a  very  long, 
slender  pseudopodium  trailing  behind  down  into  the  water  and  bent  to 
one  side.    This  pseudopodium  suddenly  swung  far  over  to  the  other  side. 

5.  Amoeba  with  many  pseudopodia  extending  in  all  directions  freely 
into  the  water.  Just  as  withdrawal  begins,  a  given  pseudopodium 
bends  over  to  one  side,  becomes  curved  to  form  a  half  circle,  or  waves 
back  and  forth  from  one  side  to  the  other. 

An  indefinite  number  of  such  observations  could  be  adduced,  showing 
that  with  its  other  movements  Amoeba  has  the  power  of  bending  and 

straightening  its  pseudopodia  and  waving 
them  from  side  to  side.  Such  movements 
have,  of  course,  been  described  by  many 
authors  ;  in  the  magnificent  monograph  of 
the  Rhizopoda  by  Penard  (1902)  many 
still  more  striking  cases  than  those  I  have 
described  are  set  forth.  Some  of  them 
should  be  quoted.  In  Amoeba  radiosa  the 
pseudopodia  ''  maybe  displaced  as  a  whole 
in  the  liquid,  and  I  have  seen  them  de- 
scribe in  this  manner  a  quarter  of  a  full 
circle  in  a  second,  like  the  handsof  a  watch 
which  one  pushes  forward  suddenly  by  fif- 
teen minutes.  On  two  or  three  occasions 
also  I  have  noticed  in  the  very  sharp  point 
of  a  pseudopodium  a  rapid  movement  of 
wave-like  vibration,  so  that  one  could  com- 
pare it  with  a  flagellum"  (/.c.,p.88).  Simi- 
lar phenomena  are  described  for  Amoeba 
Umax  (p.  36),  A.  gorgonia  (p.  79),  and 
especially  for  A,  ambulacralis  (pp.  91 ,  92), 
in  which  the  pseudopodia  act  like  tentacles. 
In  other  rhizopods,  relatives  of  Amoeba, 
Penard  describes  similar  phenomena.  Thus 
in  Pamphagus  mutabilis  (p.  439)  the  pseudopodia  are  said  to  move 
as  a  whole  in  the  water  "  almost  as  quickly  as  flagella."  Similar 
facts  are  described  for  Difflugla  pristis  (p.  2^^)^Cystodifflugia  sac- 
culus  (p.  429),  Pamphagus  granulatus  (p.  436),  Nadinella  tenella 
(p.  462),  and  various  other  rhizopods.    Penard  compares  the  movements 


Fig.  62.* 


*FiG.  62. — Movements  of  pseudopodia:  a,  a  pseudopodium  in  the  position  i 
bends  quickly  in  the  direction  shown  by  the  arrow,  and  unites  with  the  body; 
*,  a  curved  pseudopodium,  i,  straightens  into  the  position  2;  c,  the  antenna-like 
anterior  pseudopodium  of  ^w^k^^j  angulata;  it  vibrates  from  i  to  2,  thence  back 
through  I  to  3,  etc. 


THE    MOVEMENTS   AND   REACTIONS    OF  AMCEBA.  1 79 

of  the  pseudopodia  in  many  cases  to  the  vibrations  of  flagella.  Similar 
movements  of  pseudopodia  have,  of  course,  been  described  by  other 
authors,  incUiding  Butschli  (1878,  p.  272  ;  1880,  p.  123).  The  strik- 
ing resemblance  of  the  movements  of  the  pseudopodia  in  some  cases  to 
those  of  flagella  (see  especially  the  account  of  Podostoma,  Clapar^de  & 
Lachmann,  1858,  p.  441)  seems  to  indicate  that  the  motion  in  these 
two  classes  of  structures  must  be  essentially  similar  in  character,  and 
that  no  theory  of  amoeboid  movement  is  likely  to  be  correct  that  is 
inconsistent  w^ith  the  movements  of  flagella.  Certain  suggestions  as  to 
the  possibility  of  bringing  the  two  in  relation  are  given  in  the  theoretical 
portion  of  the  present  paper  (p.  218). 

The  whole  body  is  sometimes  moved  rapidly  by  such  movements  of 
the  pseudopodia.  This  happens  especially  when  the  body  is  suspended 
in  the  water  and  bears  many  long  pseudopodia,  one  of  which  comes 
in  contact  with  the  substratum.  This  pseudopodium  spreads  out  and 
extends  along  the  surface  for  a  distance,  the  part  along  the  surface 
forming  nearly  a  right  angle  with  the  free  portion.  Suddenly  the 
pseudopodium  straightens ;  since  the  distal  end  is  attached,  the  body 
is  thrown  almost  violently  against  the  substratum. 

Somewhat  similar  movements  take  place  frequently  in  Amoeba  ver- 
rucosa and  its  relatives,  without  the  formation  of  pseudopodia.  The 
course  of  events  is  usually  as  follows :  A  specimen  is  creeping  in  a 
certain  direction  in  the  usual  manner  with  the  anterior  border  attached, 
while  the  posterior  end  is  raised  a  slight  distance  from  the  substratum. 
As  a  reaction  to  stimulus,  or  for  some  other  reason,  the  anterior  end 
releases  itself  from  the  bottom.  The  posterior  end  thereupon  sinks 
down  and  becomes  attached.  Then  its  ectosarc  contracts  slightly,  in 
such  a  way  as  to  lift  the  anterior  end  suddenly.  The  animal  thus  stands 
upon  what  was  its  posterior  end.  Now,  by  varied  contractions  of  the 
parts  of  the  ectosarc  in  contact  with  the  substratum,  the  animal  may 
jerk  from  side  to  side  rapidly  and  repeatedly,  reminding  one  of  the 
movements  of  certain  caterpillars  which  jerk  their  anterior  ends  about 
in  a  similar  manner.  These  movements  are  very  striking  and  are  much 
more  rapid  than  any  that  occur  in  other  species  of  Amoeba,  so  far  as 
I  have  observed. 

The  animal  may  even  move  from  place  to  place  in  this  manner. 
Standing  on  one  end,  it  jerks  its  body  suddenly  over  to  one  side,  so  that 
the  previously  upper  end  comes  close  to  the  substratum.  This  end  now 
becomes  attached,  while  the  other  is  released.  Next  a  new  sudden  con- 
traction brings  the  released  end  upward,  so  that  the  animal  now  occupies 
a  new  location,  one  body's  length  from  that  previously  occupied.  I  have 
never  seen  the  movement  go  any  farther  than  what  I  have  just  described, 
so  that  there  is  no  evidence  that  this  method  is  employed  for  bringing 
about  orderly  locomotion. 


i8o 


THE    BEHAVIOR    OF    LOWER   ORGANISMS. 


These  movements  remind  one  of  the  ''  rolling  motion  "  described  by 
Rhumbler(i898,  p.  115)  for  these  species,  though  they  take  place  with- 
out any  noticeable  change  of  form  and  in  a  manner  entirely  different 
from  the  movements  described  by  Rhumbler.  As  we  have  seen  above 
(p.  140),  the  normal  locomotion  of  these  species  is,  in  a  certain  sense, 
of  a  *'  rolling"  character,  so  that  the  phenomena  described  by  Rhumb- 
ler as  the  rolling  movements,  perhaps  really  presented  nothing  different 
in  principle  from  the  usual  motion,  though  occurring  in  a  diflferent  way 
because  the  organism  was  unattached. 

In  addition  to  movements  of  the  character  above  described,  certain 
other  phenomena  show  in  a  different  way  the  contractility  of  the  ecto- 
sarc.  Thus,  I  stimulated  sharply  with  a  glass  rod  one  side  of  an  elon- 
gated moving  specimen  of  Amoeba 
Umax  about  one-third  its  length  from 
the  posterior  end  (Fig.  63,  a).  The 
body  at  once  contracted  rapidly,  in  a 
ring-like  manner  (^),  at  this  point, 
and  in  about  i  J  seconds  the  posterior 
portion  was  cut  off*  completely,  save 
by  a  fine  thread  (c),  by  which  it 
hung  to  the  anterior  portion  for  a 
minute  or  two.  Later  this  broke, 
and  the  posterior  piece  finally  under- 
went degeneration. 

Penard,  in  his  great  work  on  the 
Rhizopoda,  describes  similar  phe- 
nomena in  Amoeba  terricola  {ver- 
rucosa) after  injury  to  the  ectosarc. 
After  a  small  injury  the  injured  region  is  invaginated,  forming  a  small 
tube  passing  inward,  which  is  later  resorbed.  But  if  the  injury  is  large 
the  part  surrounding  it  contracts  strongly,  forming  a  deep  constriction 
between  it  and  the  remainder  of  the  body  (Fig.  64),  and  this  injured 
portion  is  finally  constricted  off* completely  (Penard,  1902,  p.  109).! 

Altogether,  then,  we  may  consider  it  thoroughly  demonstrated  that 
the  ectosarc  has  the  power  of  contracting  in  definitely  limited  regions 
in  such  a  way  as  (i)  to  produce  movements  of  entire  pseudopodia  com- 
parable to  those  of  flagella  ;  (2)  to  produce  ringlike  contractions  which 
may  even  progress  so  far  as  to  cut  the  body  in  two  completely. 

We  need  not,  therefore,  hesitate  to  admit  the  existence  of  contrac- 
tions of  the  ectosarc  in  ordinary  locomotion ;  these  are,  for  the  rest, 
as  clearly  observed  as  those  just  described. 

*FiG.  63. — An  A.  Umax  is  stimulated  strongly  near  the  posterior  end  at  a;  the 
stimulated  part  thereupon  constricts  (^,  c),  separating  off  the  posterior  end  {d), 
+  For  other  observations  on  reactions  to  injuries  see  pp.  302-204. 


Fig.  63.* 


THE   MOVEMENTS   AND    REACTIONS   OF   AMCEBA.  l8l 

REACTIONS  TO  STIMULI. 

Of  particular  importance  for  the  understanding  of  the  behavior  of 
organisms  are  those  reactions  which  determine  the  direction  of  locomo- 
tion. Experiments  show  that  the  stimuli  to  such  reactions  must,  in  a 
slow-moving  organism  like  Amoeba,  affect  only  one  side  of  the  body, 
or  at  least  affect  different  parts  of  the  body  differently.  Owing  to  the 
minute  size  of  Amoeba,  it  is  difficult  to  apply  stimuli  in  such  a  way  as 
to  fulfill  this  condition.  Heat  or  cold,  or  a  chemical  in  solution,  for 
examples,  when  applied  to  one  side  are  likely 
to  extend  to  the  other  side,  and  far  beyond, 
before  the  slow  reaction  of  Amoeba  has  taken 
place ;  the  reaction  when  it  occurs  is  then  to  a 
general,  and  not  to  a  local    stimulation.      For  ^ 

this  reason  the  reactions  of  Amoeba  to  such 
general  stimulation  are  much  better  known  than  those  to  stimuli  locally 
applied.  I  have  devoted  myself  to  the  reactions  to  localized  stimuli, 
and  have  succeeded  in  overcoming  the  experimental  difficulties  for  a 
number  of  different  classes  of  agents,  though  not  for  all. 

In  examining  the  reactions  to  stimuli,  it  will  be  necessary  to  keep  in 
mind  the  method  of  locomotion  (set  forth  briefly  on  p.  169 ;  diagram 
in  Fig.  58,  p.  170) .  The  factors  to  which  special  attention  must  be  paid 
are  :  (i)  the  sending  out  (or  rolling  over,  as  perhaps  it  would  be  better 
to  say)  of  waves  of  the  ectosarc  on  one  side,  determining  the  anterior 
end  in  the  locomotion  ;  (2)  the  atttichment  to  the  substratum  ;  (3)  the 
contraction  of  parts  of  the  body. 

The  reactions  were  studied  chiefly  in  Amoeba  proteus  and  A.  angu- 
lata;  where  other  species  were  used,  they  are  specifically  mentioned. 

REACTIONS    TO    MECHANICAL    STIMULI. 

The  reaction  to  mechanical  stimuli  may  be  either  positive  or  negative. 

POSITIVE    REACTION. 

An  Amoeba  floating  in  the  water  frequently  takes  a  starlike  form, 
with  many  long  pseudopodia  projecting  in  all  directions.  If  one  of 
these  pseudopodia  comes  in  contact  with  a  solid  object  or  the  surface 
film  (which  may  always  be  considered  a  solid  for  these  purposes) ,  the 
portion  in  contact  flattens  out,  attaches  itself  to  the  object,  and  its  proto- 
plasm begins  to  flow  out  in  a  sheet  over  the  latter.  The  other  pseudo- 
podia are  now  slowly  withdrawn  and  the  entire  animal  spreads  out  on 
the  solid,  moving  usually  in  the  direction  inaugurated  by  the  first 
pseudopodium  which  came  in  contact.  Often  in  passing  to  the  surface 
of  the  solid  there  are  a  number  of  rapid  jerking  movements,  due  to 


*FiG.  64. — A.  verrucosa  constricting  ofFan  injured  region,  after  Penard  (1902). 


l82 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


Straightening  out  or  bending  of  pseudopodia  as  described  on  p.  179. 
After  becoming  completely  transferred  to  the  surface  of  the  solid  the 
form  may  differ  much  from  that  of  the  floating  Amoeba.  Fig.  65  illus- 
trates such  a  reaction.  A  floating  Amoeba  will  thus  spread  out  on  the 
substratum,  on  the  surface  film,  or,  so  far  as  possible,  on  small  masses 
of  debris  suspended  in  the  water. 

An  Amoeba  which  is  moving  along  a  surface  also  shows  at  times  a 
positive  reaction  to  mechanical  stimuli  by  turning  toward  small  objects 
with  which  it  comes  in  contact  at  one  side  of  the  anterior  end.  This  reac- 
tion takes  place  very  frequently  in  the  normal  locomotion  of  Amoeba, 
but  I  have  not  been  able  to  produce  it  experimentally  by  touching  one 
side  of  the  animal  with  a  glass  rod.  This  is  because  it  is  difficult  to 
give  a  touch  so  light  that  it  shall  not  induce  the  negative  reaction.  I 
shall  give  a  detailed  account  of  reactions  that  probably  belong  here  in 
connection  with  the  account  of  food  reactions  (pp.  196-202,  and  Figs. 


73-76).     As  will  there  be  shown,  the  reaction  is  often  long  continued 
and  rather  complicated. 

Le  Dantec  (1895)  gave  a  good  account  of  the  positive  reaction  of 
Amoeba,  as  shown  in  its  spreading  out  on  solids. 


NEGATIVE   REACTION. 


I  have  studied  the  negative  reaction  to  mechanical  stimuli  by  touch- 
ing a  spot  on  one  side  or  end  of  the  animal  with  the  tip  of  a  fine  glass 
rod.  A  glass  rod  may  easily  be  so  drawn  out  that  its  tip  is  as  fine  as 
the  tip  of  a  pseudopodium,  and  with  some  practice  it  is  possible  to  give, 
under  the  microscope,  in  the  open  drop,  very  precisely  localized  stim- 
uli with  this. 

We  will  first  examine  the  reaction  to  a  rather  strong  stimulus  at  the 
anterior  edge  of  an  Amoeba  that  is  creeping  forward  with  outspread 
anterior  end  and  contracted  posterior  end  in  the  usual  way.  The  tip 
of  the  glass  rod  is  thrust  sharply  against  the  anterior  edge,  producing 

*  Fig.  65. — Positive  reaction  to  a  mechanical  stimulus  in  Amoeba,  in  side  view. 
A  floating  Amoeba  comes  in  contact  by  one  of  its  pseudopodia  with  a  solid  («); 
it  thereupon  passes  to  the  solid,  withdrawing  the  other  pseudopodia  {b  and  c). 
See  text. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  183 

a  depression  in  the  ectosarc  that  may  last  for  some  time  (Fig.  66). 
(We  will  suppose  that  the  thrust  does  not  detach  the  Amoeba  from  the 
surface,  as  sometimes  happens.)  At  once  the  anterior  portion  of  the 
Amoeba  ceases  to  advance.  It  remains  quiet  for  a  definite  interval, 
which  I  should  judge  to  be  about  a  second,  while  the  current  from  behind 
continues  to  move  forward.  As  a  result  of  the  stoppage  at  the  anterior 
edge  there  is  a  heaping  up  of  the  protoplasm  in  the  middle  of  the  body. 
After  about  a  second  the  part  stimulated  begins  to  contract  and,  currents 
start  backward  from  it.  Thus  the  currents  from  the  two  ends  meet  in 
the  middle,  often  producing  a  further  heaping  up  in  this  region.  Usu- 
ally, however,  the  ectosarc  of  one  side  of  the  Amoeba  quickly  gives 
way  and  a  new  pseudopodium  starts  out  laterally.  As  a  rule  this  new 
pseudopodium  is  formed  near  the  original  anterior  margin,  often  at  the 
very  edge  of  the  area  directly  affected  by  the  stimulus  (Fig.  66).  The 
reason  for  this  is  evident.  Only  this  anterior  half  of  the  Amoeba  is 
expanded  and  attached  to  the  substratum,  the  posterior  half  being  free 
and  contracted.  It  is,  therefore,  much  easier  to  continue  locomotion 
by  sending  out  pseudopodia  somewhere  in  the  attached  region  than 
behind  it.  If  sent  out  in  the  unattached  region,  the  original  contraction 
would  have  to  be  overcome,  and  no  locomotion  could  occur  until  the 
pseudopodium  had  (by  chance  ?)  come  in  contact  with  the  substratum 
and  become  attached  to  it.  By  sending  out  pseudopodia  thus  in  some 
portion  of  the  attached  region,  the  movement  is,  in  a  certain  sense,  a 
continuation  of  that  which  was  taking  place  before  stimulation,  though 
in  a  different  direction.  The  Amoeba  follows  a  path  which  forms  an 
angle  with  its  previous  one. 

The  course  of  the  reaction  may  vary  considerably  from  that  above 
described.  If  the  stimulus  is  weak  the  reaction  may  consist  merely  in 
a  stoppage  at  the  point  stimulated  without  any  contraction  there.  The 
current  from  behind  continues  ;  a  pseudopodium  breaks  out  at  one  side 
of  the  region  stimulated,  and  the  Amoeba  moves  in  the  direction  so 
indicated.  If  the  stimulus  is  very  weak  the  current  may  cease  only 
for  an  instant  in  the  region  stimulated,  then  continue  as  before ;  the 
direction  of  progress  thus  remains  unchanged. 

If  the  stimulus  is  very  strong  the  contraction  which  takes  place  at 
the  region  stimulated  may  be  very  marked,  resulting  in  the  formation 
of  strong  folds  in  this  region.  The  contraction  may  include  the  entire 
anterior  end  of  the  Amoeba.  Such  a  contraction  destroys  the  attach- 
ment to  the  substratum,  and  the  new  pseudopodium  now  bursts  out  in 
some  part  of  what  was  the  posterior  end  of  the  body.  The  new  course 
followed  may  then  be  at  right  angles  to  the  old  one,  or  at  any  greater 
angle,  or  the  course  may  be  exactly  reversed,  the  new  pseudopodium 
being  formed  at  the  posterior  end.     If  the  posterior  end  was  much 


iS4 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


wrinkled  or  bore  a  pronounced  roughened  *'  tail,"  it  is  to  be  noticed 
that  the  new  pseudopodium  does  not  flow  out  directly  from  this,  but  to 
one  side  of  it  or  above  it  (Fig.  67).  Then  as  the  AmcEba  moves  in  the 
reverse  direction  the  body  passes  the  old  '*  tail,"  which  finally  brings 
up  the  rear  again,  fusing  with  the  rough  area  produced  by  contraction  of 
the  region  stimulated  (Fig.  67,  b).  Of  course,  the  new  pseudopodium 
formed  must  come  in  contact  with  the  substratum  and  become  attached 
to  it  before  locomotion  in  the  new  direction  can  occur.  Sometimes 
the  new  pseudopodium  formed  is  sent  directly  upward  into  the  water ; 
then  there  is  no  locomotion  until  the  Amoeba  topples  over,  bringing 
the  new  pseudopodium  in  contact  with  the  substratum. 

At  times  when  the  anterior  end  is  stimulated,  two  new  pseudopodia 
are  sent  out  in  opposite  directions  on  each  side  of  the  region  stimulated. 


Fig.  66.* 


Fig.  67.1 


Both  evidently  pull  on  the  Amoeba,  which  becomes  drawn  out  to  form 
a  narrow  isthmus  between  them.    Finally  one  end  pulls  the  other  away 
from  its  attachment  to  the  bottom  ;  the  latter  then  contracts,  and  loco- 
motion continues  in  the  direction  of  the  prevailing  pseudopodium. 
There  is  at   times  a  peculiar  additional   feature  of  the  reaction  to 


*  Fig.  66. — Negative  reaction  to  a  mechanical  stimulus  in  Amoeba.  An  Amoeba 
advancing  in  the  direction  shown  by  the  arrows  is  stimulated  strongly  with  the 
glass  rod  at  the  anterior  end  (at  a).  Thereupon  the  currents  are  changed  and  a 
new  pseudopodium  sent  out  as  at  b. 

fFiG.  67. — Negative  reaction  to  a  mechanical  stimulus  when  the  anterior  end 
is  strongly  stimulated.  The  arrow,  «r,  shows  the  original  direction  of  motion ; 
the  arrows  in  a  show  the  currents  immediately  after  the  stimulation.  A  large 
pseudopodium  is  sent  out  from  above  and  to  one  side  of  the  former  tail  (/),  as  is 
shown  by  the  broken  outline.  In  b  this  pseudopodium  has  come  in  contact  with 
the  bottom ;  the  arrows  show  the  direction  of  the  currents  and  of  locomotion  at 
this  time;  /,  the  original  tail;  t\  the  new  tail  formed  by  the  contraction  of  the 
anterior  end. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  185 

strong  stimuli.  In  some  cases  there  is  for  an  instant  after  a  strong 
stimulation  at  the  anterior  end  a  sudden  rush  of  protoplasm  toward 
the  region  stimulated ;  this  is  immediately  followed  by  the  stoppage 
and  contraction  above  described.  Apparently  this  sudden  rush  toward 
the  point  stimulated  is  produced  as  follows :  The  first  effect  of  the 
additional  contraction  caused  by  the  stimulus  is  to  release  a  certain 
amount  of  surface  at  the  posterior  edge  of  the  attached  area  from  its 
attachment  to  the  substratum .  This  portion  was  nearly  ready  to  become 
released  in  the  ordinary  course  of  events,  so  that  probably  a  very  slight 
shock  would  release  it  at  once.  Now,  as  I  have  shown  on  p.  167?  when 
a  portion  of  the  lower  surface  of  the  Amoeba  is  suddenly  released  from 
the  substratum,  it  contracts,  causing  a  strong  forward  current.  This 
is  what  happens  in  the  case  under  consideration.  Later  this  current  is 
stopped  by  the  effect  of  the  stimulus  in  the  anterior  region. 

The  surface  currents  in  the  reaction  are  changed  in  the  same  way  as 
are  the  internal  currents,  and  are  throughout  congruent  with  them. 
Particles  moving  forward  on  the  upper  surface  of  the  Amoeba  stop 
after  the  stimulus,  then  move  in  the  direction  of  the  new  forward 
current.  This  has  been  illustrated  in  detail  for  Amoeba  verrucosa 
(p.  143),  so  that  we  need  not  go  into  the  matter  further  here. 

The  essential  features  of  the  negative  reaction  to  a  mechanical  stim- 
ulus are,  then,  a  contraction  of  the  region  stimulated,  with  the  formation 
of  a  new  pseudopodium  in  what  may  be  considered  the  region  of  least 
resistance,  followed  by  a  change  in  the  direction  of  the  currents  of 
protoplasm,  thus  altering  the  course  of  the  Amoeba. 

By  repeated  mechanical  stimuli  it  is  possible  to  drive  the  Amoeba  in 
any  desired  direction.  I  have  at  times  made  use  of  this  possibility  in 
order  to  bring  into  contact  two  Amoebae  or  two  pieces  of  an  Amoeba 
whose  courses  lay  in  different  directions.  Such  driving  of  an  Amoeba 
requires  considerable  skill  and  a  rather  high  tension  on  the  part  of  the 
operator.  The  new^  pseudopodium  formed  is  stimulated  to  withdraw 
as  often  as  it  is  formed,  until  it  finally  starts  out  in  the  desired  direction. 
If  it  were  possible  to  stimulate  all  of  one  side  of  an  Amoeba  at  once  it 
would,  of  course,  be  driven  directly  toward  the  opposite  side,  even 
though  the  stimulus  were  weak.  With  chemical  and  some  other  stimuli, 
as  we  shall  see,  this  is  possible.  With  mechanical  stimuli  it  is  usually 
possible  only  when  the  stimulus  is  very  strong.  By  drawing  the  tip 
of  the  glass  rod  along  one  side  of  a  moving  Amoeba,  it  is  often  possible 
to  make  it  flow  directly  toward  the  opposite  side,  as  illustrated  in  Fig. 
(i^.  This  point  is  important  for  an  understanding  of  the  effects  of  such 
stimuli  as  chemicals,  heat,  and  light. 

When  a  single  pseudopodium  is  stimulated,  it  is  merely  withdrawn, 
wrinkling  and  becoming  warty  in  the  usual  way ;  there  may  be  no 
other  effect  on  the  movement  of  the  animal. 


i86 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


Among  the  sweeping  statements  that  one  finds  current  in  regard  to 
the  behavior  of  these  low  organisms  is  one  to  the  effect  that  the  Protist 
does  not  avoid  an  obstacle  in  its  path.  This  statement  is  made  for 
example  by  Ziehen,  in  his  excellent  Leitfaden  der  physiologischen 
Psychologies*  It  is  worth  while,  therefore,  to  describe  in  connection 
with  the  reactions  to  mechanical  stimuli  just  how  Amoeba  avoids  an 
obstacle.  Let  us  take  a  concrete  case.  An  Amoeba  creeping  with  a 
broad,  flat  anterior  end  came  in  contact  at  the  middle  of  its  anterior 
edge  with  the  end  of  a  long  filament  of  some  sort  (Fig.  69).  The 
particular  spot  touched  {c)  ceased  to  move  forward,  becoming  entirely 
quiet  (reaction  to  a  weak  mechanical  stimulus).  On  each  side  of  it 
motion  continued  as  before,  so  that  after  a  time  the  filament  projected 
into  a  notch  in  the  middle  of  the  anterior  edge.     Then  gradually  the 


Fig.  68.  t 


Fig.  69.  J 


forward  movement  ceased  on  the  side  x  and  increased  at  jk,  the  pseudo- 
podium  X  contracted,  and  its  endosarc  passed  into^.  The  animal  then 
continued  its  course  in  the  direction  indicated  by  y.  It  had  thus 
changed  its  path  so  as  to  avoid  the  obstacle  presented  by  the  filament. 
Such  cases  are  often  seen. 


*  "  Hindernissen  weichen  dieselben  nicht  aus  "  (/.  c,  p.  11^. 

t  Fig.  68. — An  AmcEba  moving  in  the  direction  shown  by  the  arrows  in  the 
unbroken  outline  is  stimulated  by  drawing  the  tip  of  a  glass  rod  along  one  side, 
from  a  to  b.  Thereupon  a  pseudopodium  bursts  out  of  the  opposite  side,  as 
shown  by  the  broken  outline,  and  the  Amceba  continues  locomotion  in  the  direc- 
tion so  indicated. 

X  Fig.  69. — Method  by  which  Amceba  avoids  an  obstacle.  The  Amceba  a-b-c-d 
comes  in  contact  at  c  with  the  end  of  a  filament.  Thereupon  motion  at  c  ceases, 
while  elsewhere  it  continues,  so  that  after  a  time  the  Amoeba  has  the  position 
shown  by  the  broken  outline.  Then  the  currents  become  changed  in  x;  its  sub- 
stance passes  into  the  pseudopodium  y,  and  the  Amoeba  continues  to  move  in  the 
direction  indicated  by  the  arrows  in  the  lower  figure. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCKBA.  187 

Much  more  striking  cases  of  the  regulation  of  the  movement  in 
accordance  with  the  position  and  changes  in  position  of  outward  things 
("  automatic  acts,"  Zielien,  /.  c.)  than  are  found  in  such  a  reaction,  or 
even  than  in  the  possibility  of  driving  an  Amoeba,  will  be  described 
in  the  account  of  the  food  reactions  (p.  196). 

REACTIONS   TO   CHEMICAL   STIMULI. 

By  analogy  with  the  effects  of  mechanical  stimuli  we  might  expect 
to  find  a  positive  reaction  to  chemical  stimuli.  Such  reactions  doubt- 
less occur,  but  I  have  not  been  able  to  demonstrate  them  under  experi- 
mental conditions,  and,  so  far  as  I  am  aware,  no  one  else  has  succeeded 
in  doing  this.  Stahl  (18S4)  has  shown  the  corresponding  reaction  to 
take  place  in  the  myxomycete  plasmodium.  Verworn  (1S90,  p.  456) 
records  an  observation  which  he  refers  with  much  probability  to  a 
positive  reaction  to  a  chemical  stimulus  in  Difflugia.  If  two  conjuga- 
ting Difflugias  were  separated,  they  crept  directly  together  again,  and 
it  is  difficult  to  see  how  the  movements  could  have  been  directed  save 
by  some  chemical.  But  I  believe  there  is  no  instance  of  positive  chemo- 
taxis  in  Rhizopoda  where  the  nature  of  the  active  substance  is  known 
and  the  reaction  was  controlled  experimentally.  A  number  of  striking 
positive  reactions,  which  should  probably  be  attributed  partly  to  chemi- 
cal stimuli,  are  described  later  in  connection  with  the  attempts  of 
Amoeba  to  obtain  food  (p.  196). 

The  same  state  of  affairs  has  existed  hitherto  with  regard  to  our 
knowledge  of  a  negative  reaction  to  chemicals.  In  Amoeba  it  is,  how- 
ever, not  difficult  to  produce  such  reactions  experimentally. 

For  this  purpose  only  a  small  amount  of  the  chemical  must  be  used, 
so  that  it  can  act  on  but  a  limited  portion  of  the  body  of  the  animal. 
If  there  is  a  considerable  amount  of  the  solution,  diffusing  over  a  large 
area,  it  reaches  a  strength  sufficient  to  cause  a  reaction  at  about  the  same 
time  over  the  whole  body  of  the  Amoeba  ;  thus  the  reaction  is  a  general 
one,  not  involving  movement  in  a  definite  direction.  To  produce  a 
directed  reaction  there  must  be  a  decided  difference  in  the  strength  of 
the  solution  on  two  sides  of  the  organism. 

The  easiest  method  of  producing  the  reaction,  and  the  one  giving  at 
the  same  time  the  most  striking  results,  is  to  dip  the  moistened  tip  of 
a  capillary  glass  rod  into  powdered  methyl  green  or  methyline  blue ; 
then  to  bring  this  near  one  side  or  end  of  the  Amoeba,  in  an  open  drop 
of  water.  The  chemical  diffuses  in  a  colored  cloud  ;  the  reaction  takes 
place  when  the  edge  of  this  cloud  comes  in  contact  with  the  Amoeba. 

The  reaction  is  essentially  the  same  as  that  to  mechanical  stimuli. 
The  region  stimulated  stops  suddenly,  and  about  a  second  later  con- 
tracts, while  a  current  moves  away  from  the  side  stimulated.  This 
may  meet  the  previously  existing  current  coming  from  the  original 


l88  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

posterior  end  ;  the  two  turn  to  one  side,  and  a  pseudopodium  starts  out 

in  a  new  place.     If  the  stimulation  took  place  at  the  anterior  end  and 

was  limited  to  a  small  area,  the  new  pseudopodium  starts  out  at  one 

side  of  the  original  anterior  end  ;  the  new  course  followed,  therefore, 

forms  only  a  slight  angle  with  the  former  one  (Fig.  71,  a).     But  if  the 

stimulus  affects  all  of  one  side  of  the  body,  or  a  still  greater  portion  of 

its  area,  pseudopodia  are  sent  out  on  the  opposite  side ;  the  Amcsba 

then  creeps  directly  away  from  the  source  of  diffusion  of  the  chemical. 

This  gives  a  typical  case  of  negative  *'  chemotaxis,"  the  longitudinal 

axis  being  in  the  line  of  diffusion  of  the  ions  or  molecules,  with  the 

anterior  end  directed  away  from  the  source  of  diffusion  (Fig.  70).     It 

will  be  noted  that  the  reaction  is  exactly  the  same  as  that  produced  by 

mechanical  stimuli ;  in  "  chemotaxis,"  where  the  animal  is  ''  oriented," 

we  have  the  same  process  as  in  ''  driving"  the  Amoeba  in  a  definite 

direction  by  means  of  mechanical  stimuli.     All  movement  toward  the 

chemical  is  inhibited,  because  this  brings  the  protoplasm  into  a  region 

-«>'?^lr**"?.'-         where  it  is  stimulated.     Pseudopodia  can  be  sent  out, 

.jM^^^0^0/;i^     therefore,  only  on  the  side  away  from  the  chemical, 

Mi^s^p^Ma^i^c   and  movement  can  occur  only  m  that  direction. 

^00       The  surface  currents  are  changed  exactly  as  are  the 

internal   currents;    the  facts  here  are  identical  with 

those  described  for  mechanical  stimuli  (p.  185).    The 

^  ^  surface  currents  are  thus  awav  from  a  chemical  which 

Fig.  70.*  .  .        ,  -    ^. 

causes  a  negative  reaction  (see  Fig.  43,  p.  144). 

A  number  of  variations  in  the  reactions  to  chemicals  are  shown  in 
Fig.  71,  all  of  them  taken  from  actual  experiments.  As  the  figure 
shows,  after  stimulation  frequently  two  pseudopodia  start  out  in  oppo- 
site directions,  one  finally  prevailing  over  the  other  (Fig.  71,  d). 

The  contraction  due  to  the  chemical  is  often  very  marked,  the  ecto- 
sarc  against  which  the  chemical  impinges  shrinking  sharply  together 
and  becoming  covered  with  folds  (Fig.  71,  6).  With  methyl  green  as 
the  stimulus,  the  surface  touched  by  the  chemical  is  sometimes  stained, 
so  that  the  shrinkage  in  area  is  very  precisely  definable.  With  a  solu- 
tion of  NaCl  the  shrinkage  is  extreme,  while  the  opposite  side  spreads 
out  widely,  compensating,  or  more  than  compensating,  for  the  decrease 
in  surface  caused  by  the  shrinkage  (Fig.  71,  6). 

The  effect  of  substances  not  in  the  form  of  powder  was  tried  in  the 
following  manner :  A  glass  tube  was  drawn  out  to  a  very  fine  point, 
and  into  it  was  introduced  some  of  the  solution  to  be  tested.  The  fine 
point  of  the  tube  was  then  brought  close  to  the  Amoeba.     Some  of  the 


*  Fig.  70. — Diagram  of  "  negative  chemotaxis  "  in  Amoeba.  A  chemical  diffuses 
from  a  center,  as  indicated  by  the  radii;  the  Amoeba  reacts  in  such  a  way  as  to 
creep  directly  away  from  the  80urceofdiffusion,ina  line  with  the  radii  of  diffusion. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


189 


chemical  flowed  slowly  out,  and  its  action  on  the  Amoeba  could  be 
observed.  The  results  obtained  by  this  method  were  very  clear.  A 
negative  reaction,  as  described  above,  was  observed  in  this  way  for 
solutions  of  the  following  substances :  Methyl  green,  methyline  blue, 
sodium  chloride,  potassium  nitrate,  potassium  hydroxide,  sodium  car- 
bonate, acetic  acid,  hydrochloric  acid,  cane  sugar.  Of  these  substances 
relatively  strong  solutions  were  used  (usually  about  i  per  cent).  Of 
course,  the  solution  which  came  in  contact  with  the  Amoeba  was  much 
weaker  than  this,  being  diluted  by  the  surrounding  water.  Emphasis 
was  not  laid  on  the  quantitative  aspect  of  the  matter ;  the  question  pro- 
posed was.  How  does  the  animal  react  .^  and  not,  How  much  is  required 
to  produce  the  reaction  ?     Therefore,  different  strengths  were  employed 

:.•.v.^r_•;.•.■:v■^;••.'.•• .-.  ••  - 


Fig.  71.* 

till  one  was  found  that  was  effective.  In  any  case,  I  do  not  know  of 
any  way  in  which  one  could  determine  the  exact  strength  of  the  solution 
which  comes  in  contact  with  the  surface  of  the  Amoeba. 


*  Fig.  71. — Variations  in  reactions  of  Amoeba  to  chemicals.  The  dotted  area 
represents  in  each  case  the  diffusing  chemical.  The  arrows  show  the  direction 
of  the  protoplasmic  currents. 

a.  The  chemical  (methjl  green)  diffuses  against  the  anterior  end  of  an  advanc- 
ing Amoeba;  the  latter  reacts  by  sending  out  a  new  pseudopodium  at  one  side  of 
the  anterior  end  and  moving  in  the  direction  so  indicated. 

6.  A  solution  of  NaCl  diffuses  against  the  right  side  of  a  moving  Amoeba  (i). 
The  side  affected  contracts  and  wrinkles  strongly,  while  the  opposite  side  expands 
(2),  the  currents  flowing  in  the  direction  indicated  by  the  arrows. 

c.  A  solution  of  NaCl  diffuses  against  the  anterior  end  of  an  advancing  Amoeba. 
The  course  is  thereupon  reversed,  a  broad  pseudopodium,  shown  by  the  dotted 
line,  pushing  out  from  the  upper  surface  of  the  posterior  end  above  the  tail. 

d.  Asolution  of  methyline  blue  diffuses  against  the  anteriorendof  an  advancing 
Amoeba  (i);  thereupon  a  pseudopodium  is  sent  out  on  each  side  of  the  posterior 
end  at  right  angles  with  the  original  course  (2).  Into  these  pseudopodia  are 
drawn  the  body  and  the  tail  (3). 


190  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

As  a  control  experiment,  distilled  water  was  used  in  the  tube  in 
place  of  a  chemical  in  solution.  Amoeba  was  found  to  react  negatively 
to  this  also,  though  the  reaction  was  less  marked  than  with  most  of  the 
chemicals.  But  this  result,  of  course,  rendered  the  experiments  with 
solutions  of  chemicals  in  the  tube  indecisive,  as  the  Amoeba  may  have 
reacted  to  the  distilled  water  in  which  the*  solutions  were  made  up. 
The  solutions  were,  therefore,  made  up  with  culture  water,  and  the 
same  results  were  obtained  as  before. 

The  results  with  the  chemicals  show  merely  that  Amoeba  responds 
negatively  to  almost  any  solution  differing  markedly  from  that  in  which 
the  animal  is  immersed,  the  precise  chemical  composition  of  the  solu- 
tion being  of  little  consequence.  The  animal  responded  negatively  not 
only  to  distilled  water  and  to  the  chemicals  mentioned,  but  also  to  tap 
water,  and  to  water  taken  from  other  cultures  than  that  in  which  the 
specimens  occurred. 

REACTIONS    TO    HEAT. 

Verworn  (1889,  pp.  64-67)  studied  the  directive  influence  of  heat  on 
the  locomotion  of  Amoeba  by  concentrating  the  sunlight  on  a  small  por- 
tion of  the  slide  and  leaving  the  rest  dark,  then  observing  the  behavior 
of  the  Amoeba  on  coming  to  the  boundary  of  this  lighted  and  heated  area. 
The  effects  of  the  light  proper  were  excluded  by  control  experiments. 
It  was  found  that  on  coming  to  the  heated  area  Amoeba  remained  quiet 
a  moment,  then  contracted  on  the  heated  side,  and  sent  out  a  pseudopo- 
dium  on  the  opposite  side.  It  then  crept  away  in  the  direction  indicated 
by  this  pseudopodium  ("  negative  thermotropism"). 

My  experiments  differed  from  those  of  Verworn  in  employing  con- 
ducted heat  in  place  of  radiant  heat ;  thus  there  was  no  possibility  of 
a  complication  from  the  effects  of  light.  As  Verworn  sets  forth,  it  is 
diflScult  to  warm  only  one  side  of  so  small  an  object  as  an  Amoeba.  I 
succeeded^  however,  in  doing  this  in  a  very  sinfple  manner.  For  each 
experiment  an  Amoeba  was  selected  that  was  creeping  on  the  under 
surface  of  the  cover  glass.  This  was  placed  in  focus  under  an  objective 
of  a  considerable  focal  distance,  yet  of  high  enough  power  so  that  the 
internal  movements  could  be  seen.  A  needle  was  then  heated  in  a  flame 
and  its  point  was  brought  against  the  cover  glass  a  short  distance  in 
advance  of  the  Amoeba.  Control  experiments  had  shown  that  the  use 
of  a  needle  at  room  temperature  had  no  effect. 

If  the  heated  needle  was  placed  at  a  proper  distance  from  the  Amoeba, 
the  phenomena  follow  as  described  by  Verworn  (/.  c).  There  was  a 
short  pause,  then  the  side  next  to  the  needle  contracted.  A  current 
of  protoplasm  passed  toward  the  opposite  side,  at  times  meeting  the 
current  already  in  existence.  A  new  pseudopodium  was  sent  out,  either 
on  the  side  opposite  the  needle,  or,  in  many  cases,  in  a  direction  inter- 


THE    MOVEMENTS    AND    REACTIONS   OF   AMCEBA.  I9I 

mediate  between  this  and  the  original  one.  The  phenomena  are  in  all 
respects  identical  with  those  seen  in  the  negative  reaction  to  mechanical 
stimuli.  If  the  needle  is  brought  a  little  nearer,  so  that  the  heat  acts 
more  strongly,  there  is  a  sudden  strong  contraction  of  the  side  affected. 

Simultaneously  with  this  there  is  often,  as  in  the  case  of  strong 
mechanical  stimuli,  a  sudden  rush  of  the  internal  fluid  toward  the  side 
stimulated.  This  lasts  but  an  instant  and  is  succeeded  by  a  current 
away  from  the  stimulated  side,  the  formation  of  a  pseudopodium  on  the 
unstimulated  side,  and  locomotion  in  that  direction.  The  sudden  rush 
of  internal  contents  toward  the  side  affected  is,  I  think,  clearly  due  to 
the  cause  suggested  under  mechanical  stimuli.  Part  of  the  posterior 
portion  of  the  attached  area  of  the  Amoeba  is  loosened  from  the  substra- 
tum by  the  sudden  contraction  at  the  front  end  ;  this  portion,  therefore, 
contracts  quickly  and  sends  a  current  forward,  as  described  on  p.  168. 

When  the  heat  is  still  more  powerful  the  entire  Amoeba  is  affected. 
It  contracts  and  at  the  same  time  loses  its  attachment  to  the  substratum. 
There  is  a  strong  momentary  rush  of  the  internal  fluid  toward  the  end 
which  had  been  anterior,  due  to  the  cause  set  forth  in  the  preceding 
paragraph.  This  ceases  and  the  body  becomes  very  irregular  and  ceases 
to  move. 

The  reaction  to  local  stimulation  by  heat  is  thus  of  essentially  the 
same  character  as  the  reaction  to  mechanical  stimuli  and  to  chemicals. 

Like  Verworn  (1889,  P*  ^7)'  I  ^^^^e  been  unable  to  obtain  a  reaction 
to  cold  in  Amoeba. 

REACTIONS    TO    OTHER    SIMPLE    STIMULI. 

The  reactions  of  Amoeba  to  electricity  and  to  light  have  been  thor- 
oughly studied  by  other  authors,  so  that  it  will  not  be  necessary  to  treat 
them  in  detail  here.  Only  certain  especially  important  points  will  be 
touched  upon. 

The  reactions  of  Amoeba  to  the  continuous  electric  current  have 
been  studied  in  detail  by  Verworn  (1890,  a;  1897).  I  have  repeated  the 
experiments  in  order  to  determine  by  observation  the  direction  of  the 
surface  currents  of  protoplasm  during  the  reaction.  For  this  purpose 
soot  was  mingled  with  the  water  containing  the  Amoebae,  and  the  elec- 
tric current  was  passed  through  the  preparation.  The  typical  reac- 
tion as  described  by  Verworn  was  observed  in  many  cases,  but  the 
surface  currents,  of  course,  cannot  be  seen  unless  soot  is  resting  upon  or 
is  attached  to  the  surface  of  the  animal,  which  happens  only  rarely. 
Finally  a  specimen  of  Amceba  proteus  was  observed  with  a  string  of 
soot  particles  attached  to  one  side  (Fig.  73).  The  electric  current  was 
then  passed  through  the  preparation  in  such  a  way  that  the  side  bearing 
the  soot  was  next  to  the  anode  (Fig.  72,  a).     The  Amoeba  thereupon 


192 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


turned  and  began  to  move  toward  the  cathode  (6) ,  dragging  the  parti- 
cles of  soot  behind  it  for  a  short  distance.  Then  the  string  of  soot  began 
to  pass  forward  on  the  upper  surface,  in  the  usual  way  (c,  d).  This 
continued  until  the  soot  reached  the  anterior  edge  and  dropped  off  the 
surface  of  the  Amoeba  (e) .  The  currents  on  the  upper  surface  of  Amoeba 
are,  then,  forward  (toward  the  cathode)  in  the  reaction  to  the  electric 
current,  as  well  as  in  other  cases. 

On  reversing  the  current  the  specimen  described  above  began  to 
move  in  the  opposite  direction  toward  the  new  cathode.  In  this  and 
many  other  observed  cases  of  the  reversal  of  movement  under  the  in- 
fluence of  the  electric  current,  the  reversal  occurred  in  the  same  manner 
as  when  induced  by  other  stimuli  (see  p.  183).  That  is,  the  new  pseudo- 
podium  was  sent  out  from  one  side  of  the  attached  (anterior)  half  of  the 
body,  changing  the  course  a  certain  amount.  From  this  new  portion 
another  new  pseudopodium  was  sent  out  on  the  side  toward  the  anode, 


Fig.  72.* 

and  this  continued  until  the  direction  of  movement  had  been,  by  a 
gradual  process,  completely  reversed.  Verworn  (/.  c.)  describes  cases 
in  which  the  reversal  takes  place  suddenly,  the  new  pseudopodium 
appearing  at  the  original  posterior  end.  This  happens  also  at  times,  as 
we  have  seen,  in  the  reactions  to  other  stimuli  (p.  183).  It  is  to  be  noted 
that  the  reaction  to  the  electric  current  is  exactly  that  which  would 
occur  if  the  animal  were  strongly  stimulated  on  the  anode  side. 

Verworn  (1889),  Davenport  (1S97),  and  Harrington  &  Leaming 
(1900)  have  studied  the  reaction  of  Amoeba  to  light.  Verworn  (/.  c, 
p.  97)  found  that  light  falling  perpendicularly  on  one-half  of  the  Amoeba 
produced  no  reaction.  Davenport  (/.  c,  pp.  186,  188)  confirmed  this 
result,  but  showed  that  when  the  light  falls  obliquely  from  one  side  on 
Amoeba  the  animal  reacts  negatively.  Harrington  &  Leaming  (/.  c.) 
found  that  when  white  light  falls  upon  the  Amoeba  from  above  the 


*FiG.  72. — Movement  of  particles  attached  to  the  outer  surface  of  Amoeba  in 
the  reaction  to  the  electric  current.  Anode  and  cathode  are  represented  by  the 
plus  (-}-)  and  minus  ( — )  signs,  a,  Form  and  direction  of  movement  of  the  Amoeba 
before  the  current  is  made ;  x,  a  chain  of  soot  particles  attached  to  one  side ;  6,  c, 
d,  e,  successive  stages  during  the  reaction.  The  chain  of  soot  particles  (x)  passes 
to  the  upper  surface  and  forward,  reaching  at  e  the  anterior  edge. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I93 

movements  cease,  while  in  red  light  they  begin  again ;  lights  of  other 
colors  have  various  intermediate  effects. 

It  seems  to  the  writer  that  further  experimentation  is  desirable  on  the 
results  of  a  perpendicular  illumination  of  one-half  the  animal.  The 
difference  between  the  results  thus  far  obtained  from  such  illumination 
and  those  from  Davenport's  experiments  where  light  is  admitted  from 
one  side  is  very  remarkable.  If  this  difference  is  constant,  it  is  of  much 
significance  for  the  theory  of  light  reactions.  Possibly  the  lack  of  re- 
action when  but  one-half  the  animal  is  illuminated  may  be  accounted 
for  as  follows  :  When  one  end  of  an  Amoeba  is  illuminated  from  below, 
as  in  Verworn's  experiments,  it  is  difficult  or  impossible  to  keep  this 
difference  of  illumination  constant  for  any  considerable  period.  If  the 
Amoeba  does  not  react  at  once  it  passes  completely  into  the  lighted  area, 
where  there  is  no  cause  for  changing  the  direction  of  movement.  On 
the  other  hand,  in  the  case  of  light  falling  obliquely  from  one  side,  the 
different  action  of  the  light  on  the  two  sides  is  constant,  so  that  in  time 
a  reaction  is  produced.  The  slowness  of  Amoeba  in  reacting  is  such 
as  to  make  this  possibility  worth  considering.  For  further  work  from 
this  point  of  view  a  source  of  powerful  artificial  light  is  needed.  This 
I  have  not  had  at  command  during  the  present  investigation. 

It  is  evident  that  the  reaction  of  Amoeba  to  light  falling  from  one  side 
is  exactly  that  which  would  be  produced  were  the  Amoeba  strongly 
stimulated  on  the  side  on  which  the  light  impinges. 

For  an  account  of  the  reactions  of  Amoeba  to  general  (not  localized) 
stimuli,  see  Verworn,  1888,  and  the  Allgenieine  Physiologic  of  the 
same  author. 

SOME  COMPLEX  ACTIVITIES. 

Under  this  heading  I  propose  to  describe  certain  striking  phenomena 
in  the  behavior  of  Amoeba,  the  stimuli  to  which  are  complex  or  not 
sharply  definable.  These  concern  the  reactions  of  Amoeba  to  food  and 
to  injuries,  and  the  relations  of  one  Amoeba  to  another. 

ACTIVITIES    CONNECTED   WITH    FOOD-TAKING. 

The  behavior  of  Amoeba  in  taking  food  or  in  attempting  to  take  food 
shows  many  features  of  great  interest  for  one  attempting  to  understand 
the  behavior  of  these  organisms.  I  have  observed  the  process  of  food- 
taking  many  times,  and  will  describe  it,  together  with  a  number  of 
related  activities. 

Let  us  take  a  concrete  case.  A  specimen  oi  Amceha  proteus  was  creep- 
ing about  on  a  slide  which  contained  many  spherical  cysts  of  Euglena 
viridis.  One  of  these,  which  was  not  attached  to  the  bottom  (as  most 
of  them  are),  was  lying  in  the  path  of  the  Amoeba.  The  latter  in  its 
forward  movement  came  against  the  cyst  and  pushed  it  forward  a  short 
distance.     There  was  no  evidence  of  a  tendency  of  the  cyst  to  adhere  to 


194  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  Amoeba  ;  on  the  contrary,  it  was  pushed  ahead  as  fast  as  the  Amoeba 
moved.  The  Amoeba  now  put  out  a  pseudopodium  on  each  side  of  the 
cyst,  while  that  part  of  the  protoplasm  immediately  behind  it  stopped 
moving.  Thus  the  cyst  was  enclosed  in  a  little  bay.  On  bringing  the 
upper  surface  of  the  cyst  into  focus  it  could  be  seen  that  a  thin  layer  of 
protoplasm  was  also  sent  over  the  cyst.  The  two  pseudopodia  enclosing 
the  cyst  now  bent  over  at  their  free  ends,  so  that  the  cyst  could  not  be 
pushed  away  by  movement  of  the  Amoeba.  The  two  free  ends  finally 
met,  leaving  only  a  sort  of  transparent  seam  to  show  the  place  of  con- 
tact. Later  this  disappeared,  and  the  two  pseudopodia  fused  completely. 
At  the  end  of  two  minutes  from  the  time  that  the  Amoeba  first  came  in 
contact  with  it  the  cyst  was  completely  enclosed.  The  Amoeba  now 
remained  perfectly  quiet  for  one  minute,  then  crept  away,  carrying  the 
cyst  with  it  With  the  cyst  had  been  taken  in  some  water,  so  that  it 
was  enclosed  in  a  vacuole  a  little  larger  than  itself.  The  walls  of  the 
vacuole  had  exactly  the  appearance  of  the  ectosarc  on  the  outer  surface 
of  the  Amoeba. 

This  is  essentially  the  method  of  food  taking  that  I  have  observed  in 
a  large  number  of  cases  in  Amoeba  proteus  and  its  relatives.  The 
essential  points  are  the  sending  out  of  pseudopodia  on  each  side  of 
and  above  the  food  body  and  the  fusion  of  these  pseudopodia  at  their 
free  ends  or  edges,  thus  enclosing  the  food.  In  no  case,  in  these  species, 
was  there  any  evidence  that  the  Amoeba  was  aided  by  the  adherence 
of  the  food  body  to  its  protoplasm.  On  the  contrary,  there  was  a 
decided  tendency  for  the  food  body  to  be  pushed  away,  and  an  essential 
part  of  the  process  is  the  overcoming  of  this  mechanical  difficulty  by 
sending  out  a  pseudopodium  on  each  side  of  the  body  and  bending  the 
ends  of  them  together,  so  as  to  prevent  slipping  on  the  part  of  the 
food.*  That  this  difficulty  is  no  imaginary  one  will  be  shown  later, 
in  the  description  of  cases  where  the  Amoeba  was  unable,  after  many 
efforts,  to  enclose  the  food. 

It  is  commonly  said  that  the  posterior  rough,  tail-like  portion  of  the 
body  is  especially  important  in  the  taking  of  food,  though  it  is  sometimes 
added  that  one  rather  more  often  sees  the  partly  ingested  food  given  out 
again  in  this  region  (see  Leidy,  1879,  p.  45  ;  Penard,  1890,  p.  81  ;  1902, 
p.  16). t  I  have  never  seen  food  taken  in  at  this  part  of  the  body,  though, 
as  noted  above,  I  have  many  times  seen  it  taken  at  the  anterior  end. 
While  it  may  be  true  that  food  is  at  times  taken  at  the  posterior  end,  I 

*This  lack  of  adherence  between  the  protoplasm  and  the  food  substance  is 
emphasized  by  Le  Dantec  (1894,  p.  68;  as  a  result  of  his  careful  studies  on  food- 
taking  in  Amoeba. 

t  The  references  to  food-taking  at  the  posterior  end  seem  all  to  go  back  to  a 
paper  by  P.  M.  Duncan,  "  Studies  amongst  Amoebae,"  in  the  Popular  Science 
Review  for  1877.     I  regret  that  I  have  been  unable  to  sec  this  paper. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I95 

believe  that  the  supposed  prevalence  of  this  method  of  food-taking  and 
of  the  giving  off  of  incompletely  ingested  food  here  are  really  due  to 
incorrect  interpretation  of  another  very  common  process.  In  its  loco- 
motion Amoeba  frequently  comes  in  contact  with  diatoms,  desmids, 
encysted  Protozoa,  etc.  These  it  usually  creeps  over,  so  that  they  lie 
beneath  it  As  the  Amoeba  progresses  the  objects  come  in  contact  with 
the  posterior  portion  of  the  body,  which  is  raised  from  the  bottom  and 
covered  with  a  viscid  secretion.  Owing  to  this  viscid  substance  the 
objects  often  cling  to  the  under  surface  of  this  part  of  the  body  and  are 
carried  along  with  it.  If  observed  at  this  time  one  cannot  tell  whether 
these  objects  have  been  ingested  or  not.  But  as  a  result  of  the  method 
of  movement  of  the  Amceba  they  gradually  pass  to  the  posterior  end, 
and  are  usually  finally  left  behind.  When  such  an  object  separates  from 
the  Amoeba,  becoming  detached  from  its  under  surface,  it  appears  ex- 
actly as  if  it  were  given  off  from  within  ;  it  is  only  by  observing  the 
whole  process  from  beginning  to  end  that  one  can  be  sure  of  its  exact 
nature.  I  am  convinced  that  many  of  the  supposed  cases  of  the  inges- 
tion of  food  and  of  the  ejection  of  food  previously  ingested  at  the  poste- 
rior end  are  to  be  explained  in  this  way.  In  all  the  detailed  descriptions 
of  food-taking  in  forms  related  to  Amoeba  proteus  that  I  have  found  in 
literature,  the  food  was  taken  at  the  anterior  end  in  a  way  similar  to 
that  which  I  have  described  above  (see  Carter,  1863,  p.  45  ;  Wallich, 
1863,  c,  p.  453  ;  Leidy,  1879,  p.  49  ;  Le  Dantec,  1894,  p.  (i^) ;  also  Biit- 
schli,  1880,  p.  117). 

In  Amoeba  verrucosa  and  the  other  species  which  do  not  often  form 
pseudopodia  food  is  taken  in  a  somewhat  different  manner.  Food- 
taking  in  Amoeba  verrucosa  has  been  described  by  Rhumbler  (189S, 
p.  205).  Penard  (1902),  though  he  spent  much  time  studying  this 
species,  says  that  he  has  not  observed  the  taking  of  food,  and  thinks  it 
must  occur  only  rarely.  In  my  own  cultures  specimens  of  this  species 
taking  food  were  positively  abundant.  I  have  seen  the  process  much 
oftener  than  in  other  species.  In  A.  verrucosa  and  its  relatives  food- 
taking  is  greatly  aided  by  the  tendency  of  foreign  particles  to  cling  to 
the  surface  of  the  body,  a  tendency  which  we  found  so  convenient  for 
determining  the  movement  of  points  on  the  body  surface  (see  pp.  140- 
146).  This  adhesiveness  of  the  outer  surface  compensates  for  the  lack  of 
formation  of  pseudopodia  in  these  species.  The  outer  surface  gradually 
sinks  in  at  the  point  where  the  food  body  is  attached  to  it.  The  latter 
is  thus  carried  to  the  inside  of  the  body,  surrounded  by  a  pouch  of 
ectosarc.  This  pouch  becomes  separated  from  the  outer  ectosarc.  The 
food  is  thus  completely  enveloped  and  later  digested.  Not  only  large 
objects,  but  often  very  small  ones,  spores  of  algae,  small  diatoms,  flagel- 
lates, etc.,  are  taken  in  in  this  way.      Rliumbler  (/.  c,  p.  20S)   has 


196 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


given  a  very  interesting  account  of  the  rolling  up  and  ingestion  of  threads 
of  Oscillaria  by  this  species  (see  p.  223).* 


PURSUIT   OF   FOOD. 


Ammba  froteus  does  not  always  succeed  in  ingesting  its  food  so 
easily  as  in  the  case  just  described  (p.  194).  There  is,  as  noted  above, 
a  tendency  for  the  food  body  to  be  pushed  away  by  the  forward  move- 
ment at  the  anterior  end  of  the  Amoeba,  and  this  sometimes  gives 
serious  difficulty.  In  such  cases  Amoeba  may  show  what  would  be 
called  in  higher  organisms  remarkable  pertinacity  in  continuing   its 


Y 


^ 


Fig.  73.  t 

attempts  to  ingest  the  food.     This  will  be  illustrated  from  a  concrete 
case  (Fig.  73). 

An  Amoeba  proteus  was  creeping  toward  an  encysted  Euglena. 
The  latter  ^as  perfectly  spherical  and  very  easily  moved,  so  that  when 
the  anterior  edge  of  the  Amoeba  came  in  contact  with  it  the  cyst  merely 
moved  forward  a  little  and  slipped  to  one  side  (the  left).     The  Amoeba 


♦Leidy  (1879,  P-  86)  gives  a  very  similar  account  of  the  ingestion  of  filaments 
of  algae  in  Dinamcaba. 

tFiG.  73. — Amceba  following  a  rolling  Euglena  cyst.  Nos.  1-9  show  successire 
positions  occupied  by  Amoeba  and  cyst.     See  text  for  explanation. 


THE    MOVEMENTS    AND    REACTIONS    OP   AMCEBA.  I97 

thereupon  altered  its  course  so  as  to  follow  the  cyst  (Fig.  73,  i).  The 
cyst  was  shoved  forward  again  and  again,  a  little  to  the  left ;  the 
Amoeba  continued  to  follow.  This  continued  until  the  two  had  tra- 
versed about  one-fourth  the  circumference  of  a  circle ;  then  (at  3)  the 
cyst,  when  pushed  forward,  rolled  to  the  left  quite  out  of  contact  with  the 
Amoeba.  The  latter  then  continued  forward  with  broad  anterior  edge 
in  a  direction  which  would  have  taken  it  past  the  cyst.  But  a  small 
pseudopodium  on  its  left  side  came  in  contact  with  the  cyst.  The 
Amoeba  thereupon  turned  again  and  followed  the  rolling  cyst.  At 
times  it  sent  out  two  pseudopodia,  one  on  each  side  of  the  cyst  (as  at 
4),  as  if  trying  to  inclose  the  latter,  but  the  ball-like  cyst  rolled  so  easily 
that  this  did  not  succeed.  At  other  times  a  single  very  long,  slender 
pseudopodium  was  sent  out,  only  the  tip  of  which  remained  in  contact 
with  the  cyst  (5).  Then  the  body  of  the  Amoeba  was  brought  up  from 
the  rear  and  the  cyst  pushed  farther.  This  continued  until  the  rolling 
cyst  and  the  following  Amoeba  had  described  almost  a  complete  circle, 
returning  nearly  to  the  point  where  the  Amoeba  had  first  come  in  con- 
tact with  the  cyst.  At  this  point,  owing  to  the  form  of  the  anterior 
end  of  the  Amoeba  (7)  the  cyst  rolled  to  the  right  instead  of  to  the  left 
as  it  was  pushed  forward.  The  Amoeba  followed  (8,  9).  This  new 
path  was  continued  for  two  or  three  times  the  length  of  the  Amoeba. 
The  direction  in  which  the  ball  was  rolling  would  soon  have  brought 
it  against  an  impediment, *and  I  thought  it  possible  that  the  Amoeba 
might  succeed  in  ingesting  it  after  all.  But  at  this  point  one  of  those 
troublesome  disturbers  of  the  peace  in  microscopic  work,  a  ciliate  infu- 
sorian,  came  near  and  whisked  the  ball  away  in  its  ciliary  current. 
After  the  ball  was  carried  away  the  Amoeba  continued  to  follow  in  the 
same  direction  for  only  a  very  short  distance,  about  one-fifth  its  length, 
then  reversed  its  course  and  went  elsewhere. 

The  movements  of  Amoeba  are,  of  course,  very  slow,  and  the  behavior 
described  required  a  considerable  period  of  time — 10  or  15  minutes,  I 
should  judge.  The  whole  scene  made  really  an  extraordinary  impres- 
sion on  the  observer,  and  it  is  difficult  in  describing  it  to  refrain  from 
the  use  of  words  that  imply  a  great  deal  of  resemblance  between  Amoeba 
and  immensely  higher  organisms.  One  seems  to  see  that  the  Amoeba  is 
trying  to  obtain  this  cyst  for  food,  that  it  puts  forth  efforts  to  accom- 
plish this  in  various  ways,  and  that  it  shows  remarkable  pertinacity 
in  continuing  its  attempts  to  ingest  the  food  when  it  meets  with  diffi- 
culty. Indeed,  the  scene  could  be  described  in  a  much  more  vivid 
and  interesting  way  by  the  use  of  terms  still  more  anthromorphic  in 
tendency. 

I  have  seen  a  large  number  of  cases  like  that  above  described ;  in 
some  of  my  cultures  containing  many  specimens  of  Amoeba  proteus 


198 


THE    BKHAVIOR    OF    LOWER    ORGANISMS. 


and  many  Euglena  cysts  it  was  not  at  all  rare  to  find  the  animals 
engaged  in  thus  following  a  rolling  ball  of  food.  I  have  made  full 
notes  and  sketches  of  a  number  of  other  cases,  but  they  show  nothing 
different  in  principle  from  that  above  described,  so  that  it  is  not  worth 
while  to  enter  into  details.  One  further  point  is,  however,  worthy  of 
special  note.  Often  a  single  pseudopodium  comes  in  contact  with  such 
a  cyst  and  stretches  out  toward  it,  while  the  remainder  of  the  Amoeba 
continues  on  its  course,  away  from  the  cyst.  The  pseudopodium  in 
contact  then  stretches  out  as  far  as  possible,  keeping  in  contact  with 
the  cyst  and  often  pushing  it  ahead  (Fig.  74),  until  it  is  finally  pulled 
bodily  away  by  the  movements  of  the  whole  Amoeba.  Apparently  this 
one  pseudopodium  reacts  to  the  stimulus  quite  independently  of  the 
remainder  of  the  body.  Again,  two  pseudopodia  on  opposite  sides  of 
the  body  may  each  come  in  contact  with  a  cyst.     Each  then  stretches 


Fig.  74.* 

out,  pulling  a  portion  of  the  body  with  it,  and  follows  its  cyst,  until  the 
body  forms  two  lobes,  connected  only  by  a  narrow  isthmus.  Finally, 
one  half  succeeds  in  pulling  the  other  away  from  the  attachment  to  the 
substratum,  and  the  entire  Amoeba  follows  the  victorious  pseudopodium. 
Mechanical  stimuli  are,  of  course,  involved  in  the  above  reactions ; 
perhaps  also  chemical  stimuli  from  the  cyst.  It  is  important  from  the 
theoretical  standpoint  to  note  that  the  movement  of  particles  on  the 
surface  of  the  Amoeba  is  toward  the  object  causing  the  reaction.  This 
I  have  been  so  fortunate  as  to  have  opportunity  of  observing  in  several 
cases. 

OTHER    AMCEB^    AS    FOOD. 

Amoebae  frequently  prey  upon  each  other,  as  Leidy  has  already  de- 
scribed and  figured  (1879,  p.  94  ;  plate  7,  Figs.  12-19)  •  ^"t  the  victim 
does  not  always  conduct  itself  so  passively  as  in  the  case  described  by 
Leidy,  and  sometimes  finally  escapes  from  its  pursuer.     A  description 


♦Fig.  74. — A  single  pseudopodium  (:v)  reacts  positively  to  a  Euglena  cjst,  the 
protoplasm  flowing  in  direction  of  cyst  and  pushing  it  forward,  while  remainder 
of  the  Amceba  moves  in  another  direction  ;  1—4,  successive  forms  taken.  At  4  the 
reacting  pseudopodium  is  pulled  away  from  the  cyst,  and  then  contracts. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


199 


of  two  or  three  concrete  cases  among  those  which  I  have  observed  in 
A??iceba  angulata  will  bring  out  the  nature  of  the  behavior  under  such 
conditions.  Penard  (1902,  p.  700)  mentions  that  he  has  seen  one 
Amoeba  pursue  and  finally  capture  another,  but  does  not  give  a  detailed 
account  of  the  process. 

(i)  Two  Amoebae  were  observed,  a  large  one  and  a  small  one,  the 
former  apparently  attempting  to  swallow  the  latter  (Fig.  75).  The 
small  Amoeba  was  creeping  rapidly  forward,  while  its  wrinkled  pos- 
terior portion  was  enveloped  by  the  anterior  part  of  the  larger  Amoeba. 
The  large  Amoeba  had  the  anterior  portion  of  its  body  quite  hollowed 
out,  so   as  to  form  a  cavity  large  enough  to  contain  the  entire  small 

/ _ 

2 


Fig.  75.* 

Amoeba,  and  in  the  anterior  portion  of  this  cavity  was  inclosed  the 
hinder  portion  of  the  body  of  the  smaller  Amoeba.  Whether  this 
cavity  was  bounded  below  as  well  as  above  and  at  the  sides  by  pro- 
toplasm I  could  not  determine  with  certainty.  The  large  Amoeba  was 
following  the  small  one,  moving  at  about  the  same  rate.  There  was 
no  union  between  the  protoplasm  of  the  two  ;  on  the  contrary  the 
boundaries  of  both  were  clearly  defined,  and  they  seemed  to  be  only 
slightly  in  contact,  the  posterior  end  of  the  small  specimen  moving 
easily  within  the  cavity  of  the  other.  As  they  moved  forward,  some- 
times the  posterior  specimen  flowed  a  little  faster,  and  then  a  little 
more  of  the  smaller  one  became  enveloped  ;  at  other  times  the  smaller 
Amoeba  moved  a  little  faster,  and  then  withdrew  a  part  of  its  inclosed 

*  Fig.  75. — Pursuit  of  one  Amceba  by  another.     See  text  for  explanation. 


aOO  THE    BEHAVIOR    OF    LOWKK    ORGANISMS. 

tail.  They  progressed  in  this  fashion  for  a  long  distance,  many  times 
their  own  length.  I  watched  them  thus  for  more  than  lo  minutes. 
The  smaller,  anterior  specimen  frequently  altered  its  course ;  the 
posterior  one  followed.  I  stimulated  the  anterior  end  of  the  small 
specimen  with  the  tip  of  a  glass  rod  (Fig.  75,  3) ;  it  turned  at  a  right 
angle,  and  the  posterior  specimen  followed.  After  about  12  minutes  it 
could  be  seen  that  the  smaller  specimen  was  moving  slightly  faster 
than  the  other  and  was  slowly  withdrawing  its  posterior  end.  Finally 
it  pulled  completely  away  from  the  large  Amoeba,  which  was  still  fol- 
lowing as  rapidly  as  possible.  After  the  small  Amoeba  had  completely 
escaped  the  large  one  stopped  and  remained  entirely  quiet  for  a  few 
seconds.  The  large  cavity  in  its  anterior  portion,  which  it  had  pre- 
pared for  the  reception  of  the  small  Amoeba,  and  which  extended 
back  behind  the  middle  of  the  body,  was  still  very  evident.  After  a 
time  the  Amoeba  began  to  change  form  and  sent  out  pseudopodia 
irregularly  in  all  directions.  The  smaller  Amoeba  continued  its  for- 
ward locomotion  as  long  as  observed.  The  performance  is  illustrated 
in  Fig.  75,  from  sketches  made  while  it  was  in  progress. 

(2)  In  a  second  case  I  was  able  to  observe  the  beginning  as  well  as 
the  end  of  this  microscopical  drama  (Fig.  76).  I  had  attempted  to 
cut  an  Amoeba  in  two  with  the  tip  of  a  glass  rod,  in  the  manner  described 
later.  The  posterior  third  of  the  Amoeba,  in  the  form  of  a  wrinkled 
ball,  remained  attached  to  the  body  only  by  a  slender  cord,  the  remains 
of  the  ectosarc.  The  Amoeba  began  to  creep  away,  dragging  with  it 
this  ball.  I  will  call  this  Amoeba  a,  while  the  ball  will  be  designated  3. 
A  larger  Amoeba  (c)  approached,  moving  at  right  angles  to  the  path 
of  the  first  Amoeba ;  its  course  accidentally  brought  it  into  contact 
with  the  ball  <5,  which  was  dragging  past  its  front.  Amoeba  c  there- 
upon turned,  followed  Amoeba  a,  and  began  to  engulf  the  ball  d.  A 
large  cavity  was  formed  in  the  anterior  end  of  Amoeba  c,  reaching  back 
nearly  or  quite  to  its  middle,  and  much  more  than  sufficient  to  contain 
the  ball  d.  Amoeba  a  now  turned  into  a  new  path  ;  Amoeba  c  followed 
(Fig.  76  at  4).  After  the  pursuit  had  lasted  for  some  time  the  ball  6 
had  become  completely  enveloped  by  Amoeba  c;  the  cord  connecting 
it  with  Amoeba  a  broke,  and  the  latter  went  on  its  way  (at  5)  and  dis- 
appears from  our  account.  Now  the  anterior  opening  of  the  cavity  in 
Amoeba  c  became  partly  closed,  leaving  a  slender  canal  (5) .  The  ball  d 
was  thus  completely  inclosed,  together  with  a  quantity  of  water. 
There  was  no  union  or  adhesion  of  the  protoplasm  of  6  and  c;  on  the 
contrary  (as  the  sequel  will  show  clearly)  both  remained  quite  sepa- 
rate, c  merely  inclosing  5. 

Now  the  large  Amoeba  c  stopped,  then  began  to  move  in  another 
direction  (Fig.  76,  5-6),  carrying  with  it  its  meal.     But  the  meal,  tlie 


THE    MOVEMENTS   AND    REACTIONS   OF   AMCEBA. 


20 1 


ball  3,  now  began  to  show  signs  of  life,  sent  out  pseudopodia,  and, 
indeed,  became  very  active.  We  shall  henceforth,  therefore,  speak  of  it 
as  Amoeba  b.  It  began  to  creep  out  through  the  still  open  canal,  send- 
ing forth  its  pseudopodia  to  the  outside  (Fig.  76,  7).  Thereupon 
Amoeba  c  sent  forth  its  pseudopodia  in  the  same  direction,  and  after 
creeping  in  that  direction  several  times  its  own  length,  again  completely 


Fig.  76.* 

inclosed  b  (7-8).  The  latter  again  partly  escaped  (9),  and  was  again 
engulfed  completely  (10).  Amoeba  c  now  started  again  in  the  opposite 
direction  (i  i),  whereupon  Amoeba  b,  by  a  few  rapid  movements,  escaped 
entirely  from  the  posterior  end  of  c,  and  was  free,  being  completely 
separated  from  c  (11-12).  Thereupon  c  reversed  its  course  (12),  crept 
up  to  3,  engulfed  it  completely  again  (13),  and  started  away.    Amoeba  b 

♦Fig.  76. — Pursuit,  capture,  and  ingestion  of  one  Amoeba  by  another;  escape 
of  captured  Amoeba  and  its  recapture ;  final  escape.    See  text  for  detailed  account. 


a02  THE    BEHAVIOR   OF    LOWER    ORGANISMS. 

now  contracted  into  a  ball,  its  protoplasm  clearly  set  off  from  the  pro- 
toplasm of  its  captor,  and  remained  quiet  for  a  time.  Apparently  the 
drama  was  over.  Amoeba  c  went  on  its  way  for  about  five  minutes, 
without  any  sign  of  life  in  b.  In  the  movements  of  the  Amoeba  c  the 
ball  h  gradually  became  transferred  to  the  posterior  end  of  c,  until 
finally  there  was  only  a  thin  layer  between  b  and  the  outer  water. 
Now  b  began  to  move  again,  sent  out  pseudopodia  to  the  outside 
through  the  thin  wall,  and  then  passed  bodily  out  into  the  water  (14). 
This  time  Amoeba  c  did  not  return  and  recapture  b.  The  two  Amoebae 
moved  in  diflierent  directions  and  remained  completely  separated.  The 
whole  performance  occupied,  I  should  judge,  about  12  to  15  minutes 
(the  time  was  not  taken  till  several  minutes  after  the  beginning). 

After  working  with  simple  stimuli  and  getting  always  direct  simple 
responses,  so  that  one  begins  to  feel  that  he  understands  the  behavior 
of  the  animal,  it  is  somewhat  bewildering  to  become  a  spectator  of  so 
striking  and  complicated  a  drama.  If  we  attempt  an  analysis  of  the 
observed  behavior  of  the  Amoeba  c  into  stimuli  and  reactions,  we  ob- 
tain some  such  a  result  as  follows  :  At  first  the  stimulus  of  contact  with 
^,  and  perhaps  a  chemical  stimulus  from  the  same  source,  causes  the 
Amoeba  c  to  react  by  flowing  toward  3,  and  at  the  same  time  to  change 
form,  so  as  to  hollow  out  the  anterior  end.  Later,  every  change  in  the 
direction  of  movement  of  a  and  b  induces  a  corresponding  change  in 
the  direction  of  movement  of  c;  there  is  a  finely  co-ordinated  adapta- 
tion of  the  latter  to  the  movements  of  the  former.  After  the  separation 
of  b  from  <z,  the  movement  of  c  (at  5-6)  in  a  different  direction  may 
have  been  due  to  some  external  stimulus.  But  what  is  the  stimulus  for 
the  change  of  direction  of  locomotion  in  the  Amoeba  c  at  7  when  b  has 
begun  to  escape  ?  And  why  does  Amoeba  c  go  in  that  direction  only 
long  enough  to  get  b  firmly  inclosed  again,  then  reverse  its  course.? 
And,  finally,  why  does  Amoeba  c  reverse  its  course  at  1 1-13,  when  b  has 
entirely  escaped,  and  continue  in  this  reversed  direction  till  it  reaches 
and  recaptures  b?  The  action  is  remarkably  like  that  of  a  higher 
animal.  Doubtless  we  must  assume  chemical  and  mechanical  stimuli 
as  directives  for  each  of  the  movements  of  c,  but  the  analysis  so  obtained 
seems  not  very  complete  or  satisfactory. 

RBACTIONS    TO   INJURIES. 

Certain  cases  that  belong  under  the  heading  of  reactions  to  injuries 
have  already  been  described  as  evidences  of  the  contractility  of  the 
ectosarc ;  for  these  page  180  should  be  consulted.  The  cases  which 
we  take  up  here  are  of  a  difl^erent  character.  They  concern  Amoeba 
angulata. 

Jensen  (1896)  has  shown  in  the  case  of  certain  Foraminifera  that 
two  pieces  of  protoplasm  from  the  same  individual  will  readily  unite 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


303 


if  brought  in  contact,  while  pieces  from  different  individuals  will  not 
thus  unite.  I  was  interested  in  the  question  as  to  whether  this  would 
hold  true  also  for  Amoeba,  and  for  that  purpose  undertook  to  cut  speci- 
mens in  two.  With  the  fine  tip  of  a  glass  rod  it  is  possible,  under  the 
microscope,  in  the  open  drop,  to  cut  in  two  an  elongated  Amoeba  at 
almost  any  desired  point.  The  sharp  point  of  the  rod  is  simply  drawn 
across  the  Amoeba  as  it  lies  outspread  on  the  substratum. 

In  this  operation  it  was  found  that  the  Amoeba  was  not,  as  a  rule,  at 
first  completely  cut  in  two  by  the  stroke  itself.  The  endosarc  is  divided 
completely,  but  the  two  halves  are  still  connected  by  a  thin  layer  of 
ectosarc,  which  resists  the  cutting,  and  shows  fine  longitudinal  stria- 
tions ;  these  may  be  merely  longitudinal  folds  (Fig.  77,  2).  This  thin 
layer  of  ectosarc  seems  very  tenacious. 

2 


Fig.  77.* 

The  Amoeba  is  thus  left  in  the  condition  shown  in  Fig.  77,  2.  The 
two  halves  usually  both  contract  strongly.  Now  ensues  a  very  pecu- 
liar process.  One  of  the  two  halves  begins  to  send  out  pseudopodia 
in  such  a  way  as  to  partly  inclose  the  other  (3) ;  the  second  half  is 
thus  drawn  as  a  narrow  wedge-shaped  mass  inside  of  the  other,  as  at  4. 
It  seems  to  be  usually  the  half  that  contains  the  nucleus  that  envelopes 
the  other,  though,  as  will  be  shown  later,  the  nucleus  is  not  necessary 
for  this  reaction.  If  the  piece  thus  embraced  is  considerably  smaller 
than  the  other,  it  may  become  completely  inclosed,  and  is  then  carried 
away,  appearing  like  a  mass  of  food.  It  does  not  become  fused  with 
the  remainder  of  the  protoplasm,  but  there  is  a  sharp  boundary  between 
it  and  that  which  envelopes  it.  Specimens  were  followed  for  10  min- 
utes after  thus  inclosing  a  piece  of  their  own  bodies  ;  during  this  time 
no  marked  change  was  seen  to  occur  in  the  inclosed  piece. 

In  the  much  more  common  cases  where  the  two  pieces  are  nearly 


*FiG.  77.— Reaction  of  Amceba  to  injury.     See  text. 


204  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

equal  in  size,  or  when  it  is  the  smaller  piece  that  begins  to  envelop 
the  larger,  the  process  results  differently.  After  one  piece  has  been 
drawn  far  into  the  other  (Fig.  77,  4),  both  seem  to  contract  strongly, 
whereupon  the  connecting  band  of  ectosarc  breaks,  the  partly  inclosed 
piece  is  squeezed  out  of  the  other ;  and  the  two  separate.  Usually 
each  retains  its  form  for  a  few  seconds  after  separation  ;  one  bearing 
a  slender  truncate  pyramid  or  cone,  while  the  other  shows  a  deep 
depression  corresponding  to  this  pyramid  (Fig.  77,  5).  After  a  time 
both  halves  change  form  and  move  away.  Usually  the  half  which 
partly  inclosed  the  other  becomes  active  long  before  the  other,  but 
this  is  not  invariably  true. 

In  a  large  number  of  cases  observed  it  was  the  part  which  contained 
the  nucleus  that  attempted  to  envelop  the  other  half.  In  order  to 
determine  whether  the  nucleus  plays  a  necessary  part  in  this  perform- 
ance, I  tried  the  following  experiment:  After  the  half  which  had 
no  nucleus  had  again  become  active  and  was  moving  about,  I  cut  it  in 
two,  as  before.  Now  one  half  of  this  piece  partly  enveloped  the  other 
in  the  usual  way,  thus  showing  that  the  nucleus  is  not  necessary  for 
this  reaction. 

These  results  should  be  compared  with  Fenard's  observations  on 
injured  specimens  of  A*  terricola^  noted  on  page  180  of  the  present 
paper. 

As  to  the  question  which  these  experiments  were  originally  intended 
to  answer,  whether  two  pieces  of  a  single  Amoeba  would  reunite 
after  separation,  my  results  were  negative.  After  the  two  pieces  had 
begun  to  move  about  freely  they  were  induced  to  come  in  contact,  or 
sometimes  they  came  in  contact  accidentally  ;  but  in  no  case  was  there 
any  union.  Prowazek  (1901,  p.  93)  obtained  the  same  result  with 
small  species  of  Amoeba,  but  in  a  larger  undetermined  species  he  suc- 
ceeded in  bringing  about  a  union  of  pieces  not  only  from  the  same 
individual,  but  from  different  individuals. 

PHYSICAL  THEORIES  AND  PHYSICAL  IMITATIONS  OF 
AMCEBOID  MOVEMENTS. 

THE    SURFACE    TENSION   THEORY. 

The  movements  of  Amoeba  as  presented  by  Biitschli  (1880,  1892) 
and  Rhumbler  (1898)  (see  Figs.  30-33)  are  exactly  those  of  a  drop  of 
fluid  moving  as  a  result  of  a  local  change  in  surface  tension  (Fig.  34). 
It  was,  therefore,  natural  to  assume  that  the  cause  of  the  movements  is 
the  same  in  the  two  cases.  This  is  the  view  taken  by  the  two  authors 
named.  According  to  Biitschli,  Rhumbler,  and  many  other  authors, 
Amoeba  is  a  drop  of  complex  fluid  which  moves  about  as  a  result  of 
local  changes  in  surface  tension. 


THE    MOVEMENTS   AMD    REACTIONS    OF   AMCEBA.  205 

In  the  foregoing  investigation  it  has  been  shown  that  the  movements 
in  Amoeba  are  not  of  the  character  supposed  by  Biitschli  and  Rhumbler. 
There  is,  indeed,  very  little  resemblance  betw^een  the  movements  of 
Amoeba  and  those  of  an  inorganic  drop  moving  as  a  result  of  a  local 
change  in  surface  tension.  The  difference  is  clearly  brought  out  by  a 
comparison  of  Fig.  58,  showing  the  currents  in  Amoeba,  with  Fig.  34, 
showing  those  in  the  inorganic  drop.  The  more  striking  differences 
are  as  follows : 

(i)  In  the  drop  moving  as  a  result  of  a  local  change  in  surface  ten- 
sion the  currents  on  the  surface  are  (and  must  be)  away  from  the  side 
on  which  a  projection  is  formed  and  toward  which  the  drop  is  moving  ; 
in  the  Amoeba  the  surface  current  is  toward  this  side. 

(2)  In  the  drop  the  surface  currents  are  in  a  direction  opposed  to 
that  of  the  axial  current ;  in  Amoeba  surface  currents  and  axial  current 
are  in  the  same  direction. 

(3)  The  movement  of  Amoeba  is  in  the  nature  of  rolling,  the  upper 
surface  passing  continually  around  the  anterior  end  and  becoming  the 
lower  surface.  In  the  inorganic  drop  there  is  no  such  rolling  move- 
ment, but  the  interior  portions  of  the  fluid  are  continually  passing  to 
the  surface  at  the  anterior  end. 

Clearly,  then,  the  forces  producing  the  moyements  in  the  two  cases 
are  not  acting  in  the  same  manner.  The  locomotion  of  Amoeba  is 
demonstrably  not  due  to  a  local  decrease  in  surface  tension  on  the  side 
toward  which  the  animal  is  moving. 

This  becomes  still  clearer  when  we  consider  in  detail  the  method  by 
which  the  movements  are  produced  in  a  drop  of  inorganic  fluid  as  a 
result  of  a  local  decrease  in  its  surface  tension. 

The  phenomena  of  surface  tension  are  usually  considered  to  be  the 
result  of  the  uncompensated  attractions  of  those  particles  of  the  fluid 
which  are  near  to  the  surface.  Such  particles  are  attracted  inward  and 
laterally,  but  not  outward  (or  less  strongly  outward) .  The  resulting 
forces  may  be  considered  as  resolvable  into  two  components,  one  acting 
tangent  to  the  surface,  the  other  acting  perpendicular  to  the  surface. 
The  former  is  what  may  be  called  surface  tension  proper ;  the  latter 
is  often  spoken  of  as  normal  pressure.  The  result  is  very  much  as  if 
the  fluid  were  covered  with  a  stretched  India  rubber  membrane. 
These  relations  are  well  set  forth  in  a  recent  paper  of  Jensen  (1901). 
It  is  further  to  be  noted  that  these  two  components,  surface  tension  and 
normal  pressure,  are  two  aspects  of  one  and  the  same  thing,  and,  there- 
fore, vary  together  and  from  the  same  causes  ;  they  can  not  be  separated 
either  theoretically  or  experimentally.  Whenever  one  of  these  factors 
increases  or  decreases,  the  other  shows  a  corresponding  change.  The 
two  are  often  spoken  of  (together  with  the  pressure  due  to  curvature  of 
the  surface)  as  surface  tension  (see  Jensen,  /.  c). 


2o6  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Now,  when  the  interattraction  of  the  particles  at  a  certain  region  of 
the  surface  of  a  mass  of  fluid  is  decreased,  the  pressure  inward  and  the 
tension  along  the  surface  are  decreased.  As  the  pressure  remains  the 
same  elsewhere,  fluid  tends  to  be  pressed  out  at  the  point  where  the 
pressure  is  lowered  ;  thus  a  projection  may  be  formed  here.  As  the 
tension  remains  the  same  elsewhere,  the  remainder  of  the  surface  of 
the  drop  pulls  harder  than  that  of  the  region  under  consideration  ; 
hence  it  pulls  the  surface  of  the  fluid  away  from  the  region  where  the 
tension  is  lowered.  The  eft'ect  is  similar  to  that  which  would  be 
produced  if  one  portion  of  a  stretched  sheet  of  India  rubber  w^ere 
weakened  or  cut ;  the  remainder  of  the  sheet  would  pull  away  from  this 
region.  Thus  there  are  produced  the  currents  characteristic  of  such  a 
drop  of  fluid — an  axial  current  toward  the  region  of  lowered  tension, 
surface  currents  away  from  the  region  of  lowered  tension  (Fig.  34). 
An  increase  in  the  tension  at  the  opposite  side  would  produce  exactly 
the  same  currents,  as  Rhumbler  (1898,  p.  188)  has  set  forth,  the  axial 
current  being  always  toward  the  region  of  lowest  tension,  the  surface 
currents  in  the  opposite  direction. 

In  the  moving  Amoeba,  as  we  have  seen,  the  currents  are  by  no 
means  of  this  character.  The  axial  current  and  the  surface  current  are 
congruent,  and  both  are  in  the  direction  of  locomotion.  Such  move- 
ment could  not  be  produced  by  a  local  decrease  in  the  surface  tension 
of  some  part  of  the  body  surface. 

The  formation  of  pseudopodia  is,  as  we  have  seen,  essentially  the 
same  process  as  the  forward  movement  at  the  anterior  end  of  the 
Amoeba.  On  the  upper  surface  of  a  pseudopodium  that  is  in  contact 
with  the  substratum  there  is  a  forward  movement,  so  that  particles 
clinging  to  the  upper  surface  are  carried  over  the  tip  ;  the  currents 
which  must  result  from  a  decrease  in  surface  tension  are  not  present. 
On  the  contrary,  there  is  a  current  on  the  surface  in  the  opposite  direc- 
tion from  that  required.  The  formation  of  such  a  pseudopodium  can 
not,  then,  be  due  to  a  local  decrease  in  surface  tension. 

The  same  is  true,  essentially,  when  a  pseudopodium  is  sent  out  into 
the  water,  not  coming  in  contact  with  a  surface.  In  such  a  case,  as 
we  have  seen,  the  entire  surface  moves  outward,  in  the  same  direction 
as  the  tip  ;  there  is  no  such  backward  movement  as  the  theory  requires. 

Altogether,  it  is  clear  that  the  supposed  resemblance  between  the 
movements  and  internal  currents  of  Amoeba  and  those  of  a  drop  of  fluid 
moving  as  a  result  of  a  local  increase  or  decrease  of  surface  tension 
does  not  exist.  We  must  conclude  that  the  movements  of  Amoeba  are 
not  due  to  local  changes  in  surface  tension. 

One  might  be  tempted  to  inquire  whether  the  movement  of  Amoeba 
could  not  be  explained  by  considering  separately  the  action  of  the  two 


THE    MOVEMENTS    AXD    REACTIONS    OF    AMCEBA.  207 

factors  in  surface  tension,  the  ''surface  tension  proper"  and  the 
"  normal  pressure.'*  If  the  normal  pressure,  directed  inward,  were 
decreased  in  a  certain  region,  while  the  tangential  factor,  the  ''surface 
tension  proper,"  were  not  decreased,  were  perhaps  even  increased, 
could  not  pseudopodia  be  formed  as  actually  occurs,  without  any  back- 
ward current  on  the  surface?  Jensen  seems  to  lean  toward  the  possi- 
bility of  such  action  when  he  speaks  of  the  variation  of  one  of  these 
factors  without  the  other  (Jensen  1901,  p.  374).* 

But  with  such  an  inquiry  should  we  not  leave  the  field  of  realities  to 
wander  among  abstractions  ?  One  who  is  not  a  physicist  can,  of  course, 
not  speak  positively  on  such  a  point.  Yet,  so  far  as  I  am  able  to  dis- 
cover from  the  results  of  experiments  and  from  the  theories  of  surface 
tension,  the  state  of  the  case  is  about  as  follows  :  The  tangential  tension 
and  the  normal  pressure  are  not  two  different  things ;  they  are  only 
different  aspects  of  one  and  the  same  thing.  Viewed  from  the  stand- 
point of  "  energetics,"  what  the  physical  experiments  show  liquids  to 
possess  is  surface  energy,  in  virtue  of  which  they  tend  to  decrease  their 
surface  and  resist  an  increase  of  surface,  however  these  changes  are 
brought  about  (see  Ostwald,  1902,  p.  197).  When  the  "  surface  ten- 
sion is  decreased"  in  a  certain  region  (x)  of  a  fluid  mass,  this  signifies  that 
the  tendency  to  a  decrease  of  surface  and  the  resistance  to  an  increase 
of  surface  is  lessened  in  this  region.  As  a  result,  the  remainder  (y)  of 
the  fluid  decreases  its  surface  at  the  expense  of  the  region  x;  the  latter 
is  thus  compelled  to  increase  its  surface.  This  takes  place  by  simulta- 
neous passage  of  the  contents  of  y  into  x  and  of  the  surface  of  a:  on  to 
y,  the  two  operations  being  essentially  one,  and  both  having  the  result 
of  decreasing  the  surface  of  ^  and  increasing  that  of  x.  There  would 
seem  to  be  no  ground,  theoretical  or  experimental,  for  supposing  that 
in  a  fluid  one  of  these  operations  could  take  place  without  the  other. 
An  attempted  explanation  of  this  sort  would  be,  if  these  considerations 
are  correct,  not  a  physical  explanation,  but  a  purely  hypothetical  one, 
working  with  conditions  not  known  to  exist.  The  whole  value  of  the 
surface  tension  theory  lies  in  its  direct  reference  back  to  the  results 
of  physical  experiments — in  its  fidelity  to  the  results  of  such  experi- 
ments. As  soon  as  it  leaves  this  ground  it  becomes  of  no  more  value 
than  the  thousand  and  one  other  hypotheses  that  have  been  constructed 
for  the  explanation  of  contractility. 

Further,  even  this  purely  hypothetical  explanation  could  not  account 
for  the  forward  currents  on  the  upper  surface  of  Amoeba,  nor  for  the 
transference  of  portions  of  the  body  surface  to  the  surface  of  a  pseudo- 
podium.  In  any  form  we  can  give  it,  the  theory  that  the  movement  is 
due  to  local  changes  in  surface  tension  is  not  in  agreement  with  the 
observed  phenomena. 

*  Though  elsewhere  he  speaks  of  the  necessity  of  their  varying  together. 


2o8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

BERTHOLD's     theory     that     ONE-SIDED     ADHERENCE    TO     THE     SUB- 
STRATUM   IS    THE   CAUSE   OF    LOCOMOTION. 

If,  then,  the  movements  of  Amoeba  are  not  due  to  local  decrease  in  sur- 
face tension,  with  the  formation  of  " Ausbreitungscentren  "  (Biitschli), 
is  it  possible  to  find  a  physical  explanation  for  them  ?  In  taking  up 
this  question  we  must  consider  separately  (i)  locomotion,  and  (2)  the 
formation  of  pseudopodia. 

Observation  and  experiment  indicate,  as  we  have  seen  in  the  obser- 
vational portion  of  this  paper,  that  Amoeba  is  a  drop  of  fluid  which 
becomes  attached  to  the  substratum  in  front  and  pulls  itself  forward, 
the  pull  extending  backward  from  the  attached  region  over  the  upper 
surface,  and  producing  a  rolling  motion. 

Now,  a  drop  of  inorganic  fluid  under  the  influence  of  similar 
forces  moves  in  precisely  the  same  manner.  There  is  no  great  difl[i- 
culty  in  causing  a  drop  of  inorganic  fluid  to  adhere  more  strongly  to 
the  substratum  on  one  side  than  elsewhere.  When  this  is  brought 
about  the  drop  moves  toward  the  more  adherent  side  by  a  rolling 
motion,  precisely  like  that  of  Amoeba.  By  a  proper  arrangement  of 
the  conditions  almost  every  detail  of  amoeboid  locomotion  may  be 
closely  imitated. 

That  this  is  the  method  of  movement  in  Amoeba  was  the  theory 
maintained  by  Berthold  (1886),  though  it  is  rather  curious  that  the 
supposed  facts  on  which  he  based  this  view  were  incorrect.  Berthold 
confirmed  on  the  basis  of  observations  on  Amoeba  verrucosa  (  ! )  and 
other  species  the  account  of  the  currents  in  Amoeba  given  by  Schulze 
(see  p.  137  and  Fig.  37)  ;  that  is,  such  currents  as  would  be  consistent 
with  the  theory  of  local  decrease  in  surface  tension,  but  are  quite  incon- 
sistent with  his  own  theory.  He  rejected  the  theory  that  locomotion  is 
due  to  a  decrease  in  surface  tension  at  the  anterior  end,  on  the  ground 
that  no  currents  are  to  be  observed  in  the  surrounding  water,  as  this 
theory  demands.  Berthold  held  that  the  locomotion  is  due  to  the 
spreading  out  of  the  anterior  end  of  the  fluid  mass  on  the  surface  of  a 
solid,  this  spreading  out  being  due  to  adhesion  between  the  fluid  and 
the  solid.  Unfortunately  for  the  understanding  of  his  theory,  he  tried 
to  bring  this  into  relation  with  many  other  much  less  simple  phenom- 
ena. In  particular  he  compared  the  movements  to  those  of  a  drop  of 
water  on  a  glass  plate,  which  flees  when  a  rod  wet  with  ether  is  brought 
near  one  side.  This  was  an  unfortunate  comparison,  as  the  movements 
in  a  drop  of  water  under  such  circumstances  are  of  a  character  entirely 
different  from  those  produced  when  a  mass  of  fluid  adheres  by  one  side 
to  a  solid.  The  movement  in  a  drop  of  water  fleeing  from  the  ether- 
ized rod  is  a  result  of  the  currents  produced  by  the  lowering  of  the 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  2O9 

surface  tension  on  one  side,  as  Biitschli  (1S92,  pp.  191  and  194),  has 
shown.  This  comparison,  and  Berthold's  discussion  of  the  relations 
between  spreading  out  on  the  surface  of  solids  and  on  the  surface  of 
liquids,  together  with  his  incorrect  idea  of  the  currents  in  such  spread- 
ing out  on  a  solid,  have  served  to  distract  the  attention  of  investigators 
from  the  really  simple  essential  features  of  such  a  theory.  Berthold 
did  not  attempt  to  study  directly  the  currents  and  other  movements  of 
a  drop  of  fluid  moving  as  a  result  of  one-sided  adherence  to  a  solid. 
We  may,  therefore,  leave  his  account  and  examine  for  ourselves  the 
phenomena  in  question. 

EXPERIMENTAL    IMITATION   OF   THE    LOCOMOTION    OF   AMCEBA. 

The  experiments  with  inorganic  fluids  may  be  performed  as  follows  : 
A  piece  of  smooth  cardboard,  such  as  the  Bristol  board  used  for  drawing, 
is  placed  on  the  level  bottom  of  a  shallow  vessel,  such  as  a  Petrie  dish, 
and  soaked  with  bone  oil  by  spreading  the  latter  over  its  surface.  A 
small  area  on  the  surface  of  the  board  is  protected  from  the  oil  by 
placing  upon  it  a  drop  of  water.  After  the  board  has  become  well 
soaked,  the  drop  of  water  is  removed  with  a  pipette,  leaving  this  spot 
merely  damp,  while  a  layer  of  oil  some  millimeters  deep  is  poured  into 
the  vessel,  covering  the  cardboard  completely.  A  drop  of  glycerine  or 
of  water  is  then  introduced ;  this  settles  to  the  bottom,  but  adheres  to 
it  only  slightly.  A  drop  of  glycerine  is  in  some  respects  preferable,  as 
its  movements  are  slower.  To  the  drop  should  be  added  beforehand  a 
quantity  of  soot,  in  order  to  make  its  internal  movements  visible. 
Some  of  the  soot  remains  on  the  surface,  projecting  out  into  the  oil, 
thus  making  it  possible  to  observe  the  surface  currents. 

If  the  drop  is  brought  close  to  the  spot  on  the  cardboard  that  was 
protected  from  the  oil,  so  that  one  side  comes  in  contact  with  this 
region,  the  edge  of  the  glycerine  or  water  drop  spreads  out  over  this 
area.  Thereupon  the  remainder  of  the  drop  is  pulled  in  that  direction, 
till  the  whole  drop  takes  up  its  position  over  the  protected  spot.  In 
the  movement  of  the  drop  toward  the  area  to  wliich  one  side  adheres, 
it  rolls  exactly  as  Amoeba  does.  The  currents  on  the  upper  surface 
and  within  the  drop  are  forward.  Toward  the  sides  the  currents  are 
somewhat  less  marked,  and  on  the  under  surface  they  cease  entirely; 
particles  within  the  drop  but  in  contact  with  the  lower  surface  are  not 
moved  at  all.  The  forward  current  is  most  rapid  in  front,  becoming 
slower  at  the  rear,  exactly  as  in  Amoeba.  At  the  posterior  end  the 
surface  rolls  upward ;  particles  on  the  surface  which  were  at  first  on 
the  bottom  may  be  seen  to  pass  upward  around  the  posterior  end  and 
then  forward,  as  in  Amoeba.  The  form  of  the  drop  may  become  much 
elongated;  the  anterior  edge  is  thin,  the  posterior  end  thick  and 
rounded.     In  all  these  respects  the  drop  resembles  the  moving  Amoeba. 


2IO  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

By  inclining  the  vessel  the  drop  may  be  made  to  roll  away  from  the 
attractive  spot;  then  when  the  level  is  restored  it  moves  back  again. 
By  repeating  this  process  the  movements  may  be  studied  in  detail. 
For  studying  the  movements  in  all  parts  except  at  the  anterior  edge 
another  more  convenient  method  may  be  employed.  A  small  piece  of 
wood  may  be  brought  against  one  side  of  the  drop  ;  toward  this  it 
moves  in  the  manner  just  described.  If  the  piece  of  wood  is  moved 
continually  in  a  certain  direction,  the  drop  follows,  and  its  movements 
may  be  examined  with  ease.  In  this  case  the  anterior  edge,  of  course, 
is  not  thin  and  pressed  against  the  surface,  but  otherwise  the  move- 
ments are  the  same. 

By  proper  modifications  further  details  of  the  movement  of  Amoeba 
are  exactly  imitated.  Thus  a  quantity  of  sand  grains  or  other  heavy 
objects  may  be  added  to  the  drop.  In  the  movement  these  collect  at 
the  posterior  end,  as  happens  with  the  coarse  internal  contents  in 
Amoeba.  A  large,  spherical  bubble  of  oil  may  be  introduced  into  the 
drop,  in  imitation  of  the  contractile  vacuole ;  this  likewise  stays  near 
the  posterior  end.  When  a  considerable  quantity  of  heavy  material  is 
collected  at  the  posterior  end,  the  latter  becomes  drawn  out  into  a  sort 
of  pouch,  which  is  dragged  along,  its  substance  not  partaking  of  tlie 
currents  shown  by  the  remainder  of  the  drop.  It  thus  plays  the  same 
part  as  the  well-known  posterior  appendage  of  Amoeba.  Material 
passes  up  from  the  bottom  to  the  upper  surface  on  each  side  of  this 
posterior  pouch,  just  as  happens  in  Amoeba  (see  p.  i68).  Particles 
clinging  to  the  outer  surface  at  the  posterior  end  are  often  dragged 
along  for  a  considerable  time,  then  finally  pass  upward  to  the  upper 
surface  and  so  forward,  exactly  as  described  for  Amoeba  (p.  169).* 

In  another  detail  the  movements  of  the  drop  of  water  or  glycerine 
are  strikingly  like  those  of  Amoeba.  As  we  have  seen,  the  current  is 
most  rapid  at  the  anterior  end  in  both  cases,  becoming  as  a  rule  slow 
toward  the  rear.  But  I  have  pointed  out  that  in  Amoeba  the  move- 
ments at  the  posterior  end  are  not  uniform.  Sometimes  the  under  sur- 
face remains  attached  to  the  bottom  longer  than  usual,  then,  when  it 
becomes  detached  over  a  considerable  area  at  once,  there  is  a  sudden 
rush  of  the  fluid  forward  from  the  posterior  region  (p.  16S).  Exactly 
the  same  thing  is  to  be  observed  in  the  inorganic  drop.  The  bottom 
is  not  uniform,  so  that  sometimes  the  posterior  end  clings  to  it  longer 
than  usual ;  this  end  is  then  drawn  out,  and  when  it  is  finally  released 


*It  maybe  worthwhile  to  state  that  these  experiments  on  inorganic  fluids 
were  performed  after  the  work  on  the  movements  of  Amoeba  had  been  completed 
and  the  description  entirely  written  in  the  form  given  in  the  preceding  pages. 
No  details  of  the  movements  of  Amoeba  were  added  after  the  behavior  of  the 
inorganic  drops  had  been  studied. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  211 

there  is  a  sudden  rush  forward  of  the  internal  fluid  from  this  region, 
giving  the  movement  a  jerky  character. 

Still  another  resemblance  in  detail  between  the  movements  of  the 
inorganic  drop  and  of  Amoeba  may  be  noted  at  times.  As  we  have 
seen,  in  the  posterior  part  of  Amoeba  that  is  detached  from  the  bottom 
there  is  a  movement  forward  not  only  on  the  upper  surface,  but  also  a 
slow  movement  on  the  lower  surface  ;  the  entire  posterior  region  is 
contracting.  The  same  thing  may  be  seen  in  the  inorganic  drop.  The 
phenomenon  in  question  is  not  so  regular  here,  because  the  posterior 
half  usually  still  clings  to  the  surface  to  a  certain  extent,  while  in  Amoeba 
it  is  as  a  rule  entirely  free.  But  when  the  posterior  half  of  the  inor- 
ganic drop  does  become  entirely  free,  it  is  seen  to  contract  as  a  whole, 
with  a  forward  movement  on  both  upper  and  lower  surfaces,  exactly 
as  in  Amoeba. 

One  may  even  see  at  times,  under  special  conditions,  a  slight  turning 
backward  of  the  current  at  the  sides  of  the  anterior  end,  such  as  has 
been  described  by  a  number  of  authors  for  Amoeba  (see  p.  137).  This 
occurs  when  the  drop  is  slender  and  elongated,  and  the  area  on  which 
it  spreads  out  is  broad.  On  coming  in  contact  with  the  area,  the  end 
of  the  drop  rushes  forward  and  spreads  out.  If  the  whole  width  of  the 
area  is  not  covered  at  first,  some  of  the  particles  that  have  moved  for- 
ward curve  outward  and  a  little  backward  till  the  area  is  quite  covered. 

Altogether,  the  resemblance  between  the  movements  of  the  inor- 
ganic drop  and  those  of  Amoeba  is  extraordinary,  extending  even  to 
details.  What  are  the  forces  at  work  in  such  a  drop,  and  in  how  far 
may  they  be  supposed  to  be  active  also  in  Amoeba? 

The  spreading  out  of  the  drop  of  glycerine  or  water  at  the  anterior 
end  is  due  to  its  adherence  here  to  the  substratum.  The  remainder  of 
the  movements  of  the  inorganic  drop  are  due  to  the  interplay  of  surface 
tension  and  adhesion  to  the  substratum.  As  a  result  of  surface  tension 
the  drop  seeks  to  regain  its  spherical  form  ;  hence  the  posterior  part  is 
pulled  forward,  the  force  required  to  accomplish  this  being  less  than 
would  be  demanded  for  freeing  the  anterior  edge  from  the  substratum. 
In  the  pulling  forward  of  the  posterior  portion  the  adherence  of  the 
lower  surface  to  the  bottom  keeps  this  surface  from  moving ;  hence  the 
upper  surface  moves  forward  while  the  lower  surface  remains  quiet 
or  moves  forward  only  very  slowly ;  the  movement  is  thus  converted 
into  a  rolling  motion.  The  details  given  above  depend  merely  upon 
the  relative  part  played  by  adherence  and  surface  tension,  with  the 
resistance  offered  by  the  weight  and  inertia  of  particles  inclosed  in  the 
drop. 

In  Amoeba,  so  far  as  the  evidence  of  observation  goes,  the  conditions 
are  similar.     Amoeba  adheres  to  the  substratum  and  spreads  out  in  a 


212  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

similar  manner.  In  one  respect  there  is,  of  course,  a  striking  differ- 
ence between  the  two  cases.  Amoeba  does  not  require  that  the  sub- 
stratum should  be  different  on  its  two  sides  in  order  that  there  should 
be  movement ;  on  the  contrary,  it  may  move  steadily  in  a  certain  direc- 
tion on  a  uniform  surface.  The  mechanism  of  the  movement  might, 
nevertheless,  be  the  same  as  in  the  inorganic  drop.  Chemically  different 
substances  show  different  degrees  of  adherence  to  the  same  surface.  It 
may  be  supposed,  therefore,  that  there  is  a  chemical  difference  between 
the  anterior  and  posterior  regions  of  Amoeba  of  such  a  nature  that  the 
anterior  region  clings  to  the  surface  while  the  posterior  region  does  not. 
This  chemical  difference  must,  of  course,  be  continually  renewed,  since 
new  parts  of  the  body  continually  come  in  contact  with  the  substratum. 

It  may,  however,  be  questioned  whether  the  adhesion  of  Amoeba  to 
the  substratum  is  of  the  same  character  as  the  adhesion  of  a  drop  of 
water  to  glass  ;  in  other  words,  whether  Amoeba  really  plays  here  the 
part  of  a  fluid,  and  "  wets"  the  substratum.  This  was  the  view  taken 
by  Berthold  (1886)  and,  if  I  understand  him  correctly,  Le  Dantec 
(1895).  Apparently  opposed  to  such  a  view  is  the  fact  that  Amoeba 
may  creep  on  the  under  side  of  the  surface  film  of  water,  as  I  have 
often  observed.  This  surface  film  is,  of  course,  fluid  ;  if  in  adhesion 
Amoeba  itself  also  plays  the  part  of  a  fluid,  we  should  have  two  fluids 
in  contact,  having  the  same  relation  of  attraction  or  adhesion  that  a 
fluid  has  for  a  solid  that  it  "  wets"  ;  that  is,  the  particles  of  each  fluid 
have  a  greater  attraction  for  those  of  the  other  fluid  than  for  each  other. 
This,  it  would  appear,  could  result  only  in  the  formation  of  diffusion 
currents  in  the  two  fluids  ;  the  two  would  mix.  This  result  does  not 
follow,  so  that  it  would  appear  that  in  adhesion  Amoeba  does  not  play 
simply  the  part  of  a  fluid  which  wets  the  substratum.  As  we  have 
seen  (p.  165),  there  is  evidence  that  the  adhesion  takes  place  through 
the  mediation  of  a  viscid  secretion. 

Whatever  the  nature  of  the  adhesion,  we  know  it  exists  at  one  pole 
of  the  Amoeba  and  not  at  the  other.  Given  such  chemical  differences 
between  the  two  poles  as  would  produce  this  difference  in  adhesion, 
then  locomotion  would  follow  essentially  as  we  find  it  to  occur  in 
Amoeba  Umax  or  A.  verrucosa.  No  further  properties  except  those 
common  to  fluids  would  be  required.*  For  the  determination  of  the 
direction  and  rate  of  locomotion,  the  distribution  of  these  chemical 
differences  would  be  the  essential  factor. 

Caution  is  necessary,  however,  in  transferring  the  results  of  these  and 
other  similar  experiments  to  Amoeba.  The  resemblances  between  the 
movements  of  the  inorganic  drops  and  those  of  Amoeba  show  merely 

♦It  will  be  noted  that  this  statement  is  made  for  simple  locomotion,  and  does 
not  refer  to  the  formation  of  pseudopodia. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  2I3 

that  the  forces  acting  upon  the  two  have  a  similar  localization  and 
direction,  not  necessarily  that  the  forces  themselves  are  identical.  This 
caution  is  emphasized  by  the  fact  that  drops  moving  down  an  inclined 
plane  as  a  result  of  the  action  of  gravity  have  a  similar  rolling  motion. 
This  is  well  shown  in  the  drops  of  glycerine  or  water  on  the  oiled 
surface,  in  the  experiments  just  described.  Most  (though  not  all)  of 
the  details  mentioned  above,  in  which  the  movements  of  the  inorganic 
drop  resemble  those  of  Amoeba,  may  be  observed  also  in  drops  moving 
under  the  influence  of  gravity.  The  essential  difference  between  the 
two  sets  of  experiments  is  that  the  action  of  adhesion,  pulling  the  drop 
in  a  certain  direction  in  the  one  case,  is  replaced  by  the  action  of 
gravity,  pulling  in  the  same  direction,  in  the  other  case.  Correspond- 
ing with  this  difference  is  the  chief  difference  to  be  observed  in  the 
movements  of  the  drops  under  the  different  conditions.  In  those  mov- 
ing as  a  result  of  greater  adhesion  on  one  side,  the  anterior  edge  is 
thin  and  flat,  as  in  Amoeba,  while  in  those  moving  from  the  action  of 
gravity  this  is  not  true. 

In  Amoeba  observation  shows  that  we  have  the  one-sided  greater 
adhesion,  and  the  tendency  of  the  lower  surface  to  cling  slightly  to  the 
substratum,  as  in  the  first  set  of  experiments  with  the  inorganic  drops. 
There  remains  only  something  corresponding  to  the  surface  tension 
factor,  common  to  both  sets  of  inorganic  experiments,  to  be  accounted 
for  in  Amoeba.  Since  Amoeba  acts  like  a  fluid  in  many  respects,  there 
is  no  a  -priori  reason  to  deny  it  surface  tension,  and  nothing  further  is 
required  to  produce  locomotion.  To  this  there  is,  however,  one  objec- 
tion. This  is  found  in  the  roughening  and  wrinkling  of  the  surface 
at  the  posterior  end  as  it  contracts,  and  in  the  similar  roughening  of  a 
contracting  pseudopodium  (pp.  i6o,  i68) .  This  is  exactly  the  opposite 
of  what  should  take  place  in  a  fluid  contracting  as  a  result  of  surface  ten- 
sion. In  such  a  case  the  primary  phenomenon  is  the  decrease  in  sur- 
face ;  the  latter  should,  therefore,  remain  perfectly  smooth,  and  as  small 
as  possible.  Of  course,  surface  tension  might  be  replaced  in  Amoeba 
by  a  specific  property  of  contractility  of  some  sort,  having  its  seat  a 
little  beneath  the  surface.  Locomotion  would  then  take  place  as  in 
the  inorganic  drop,  and  the  wrinkling  of  the  outer  surface  would  be 
accounted  for.  On  the  other  hand,  if  we  can  account  for  the  contrac- 
tility by  a  known  property  of  fluids,  such  as  surface  tension,  our  expla- 
nation will,  of  course,  be  simpler  and  more  probable.  By  taking  into 
consideration  the  apparent  fact  that  the  outer  layer  of  Amoeba  is  partly 
fluid,  partly  solid,  I  believe  that  such  an  explanation,  accounting  for 
the  roughening  as  well  as  the  contractility,  can  be  given  ;  this  I  shall 
attempt  in  the  next  section  of  this  paper  (p.  215). 

The  formation  of  projections  at  the  anterior  edge  or  side  of  the  inor- 
ganic drop,  comparable  to  the  formation  of  pseudopodia  in  contact  with 


214  '^^^    BftHAVlOR    OF    LOWER    ORGANISMS. 

the  substratum  in  Amoeba,  may  also  be  induced  in  the  oil  drops.  For 
this  purpose  it  is  necessary  to  produce  a  greater  adhesion  on  a  small 
area  at  one  side.  A  projection  is  at  once  sent  out  here.  The  move- 
ment in  sending  out  such  a  projection  is  the  same  as  that  to  be  observed 
in  the  formation  of  a  pseudopodium  under  such  circumstances.  The 
projection  is  thinnest  at  the  tip  ;  its  upper  surface  moves  forward  and 
rolls  over  at  the  point,  while  the  lower  surface  is  at  rest. 

FORMATION    OF   FREE   PSEUDOPODIA. 

On  the  other  hand,  the  projection  of  free  pseudopodia  into  the  water 
cannot  be  imitated  under  these  conditions.  As  we  have  seen,  the  move- 
ment in  the  formation  of  a  free  pseudopodium  differs  from  that  in  form- 
ing a  pseudopodium  along  a  surface  merely  in  the  fact  that  in  the  latter 
case  the  contact  surface  is  at  rest,  while  in  the  free  pseudopodium  all 
surfaces  move  equally,  a  given  point  on  the  surface  remaining  approx- 
imately at  the  same  distance  from  the 'tip.  In  the  inorganic  drop  pro- 
jections can  indeed  be  formed  in  which  the  surface  moves  in  exactly 
the  same  manner  as  in  the  free  pseudopodia  of  Amoeba,  but  under  con- 
ditions that  are  essentially  different.  If  some  small  object  to  which  the 
fluid  adheres,  such  as  a  sliver  of  wood,  is  brought  into  contact  with  one 
side  of  the  drop,  the  fluid  flows  out  over  it,  and  may  form  thus  a  long, 
slender  projection.  The  surface  of -this  projection  moves  in  the  same 
manner  as  the  surface  of  a  pseudopodium  in  Amoeba  (p.  153).  Thus 
the  surface  of  a  free  pseudopodium  shows  such  movements  as  it  would 
if  drawn  out  by  an  object  to  which  it  adheres  at  its  tip.  Since  no  such 
object  is  present,  it  is  clear  that  the  formation  of  free  pseudopodia  is  not 
explicable  in  this  manner. 

As  we  have  seen  above,  the  locomotion  and  the  formation  of  pseudo- 
podia in  contact  with  the  substratum  could,  if  they  stood  alone,  be  con- 
sidered due  to  the  adherence  and  spreading  out  of  a  fluid  on  a  solid,  as 
maintained  by  Berthold  (1886).  But  they  do  not  stand  alone  ;  we  have 
the  additional  fact  that  pseudopodia  may  be  sent  out  which  are  not  in 
contact  with  the  substratum.  The  anterior  edge  of  an  Amoeba,  further, 
may  be  pushed  out  freely  into  the  water  as  a  single  pseudopodium. 
This  may  frequently  be  seen  in  Ammba  Umax.  As  a  reaction  to  a 
stimulus  the  protoplasm  may  push  upward  freely  as  a  thick  lobe,  till 
the  greater  part  of  the  substance  is  transferred  upward  and  the  Amoeba 
topples  over  (p.  184) .  In  the  formation  of  such  a  lobe,  the  protoplasm 
may  flow  from  both  ends  toward  the  middle,  producing  the  *'  heaping 
up'*  from  which  the  thick  upward  projection  results  (see  p.  183). 
Currents  flowing  in  this  manner  could  not  possibly  be  produced  by 
adherence  to  the  substratum.  Again,  in  an  advancing  Amoeba  angzi- 
lata^  short  triangular  pseudopodia  are  constantly  pushed  forward,  some 
in  contact  with  the  substratum,  others  not  thus  in  contact,  but  raised  a 


THK    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  315 

little  above  it  (Fig.  54).  Some,  which  are  at  first  free,  later  come  in 
contact.  Clearly,  Amceifa  is  able  to  -perform  all  the  activities  con- 
cerned in  locomotion  without  adherence  to  a  solid.  The  adherence 
is  only  necessary  that  there  may  be  a  movement  from  place  to  place. 
The  case  is  quite  parallel  to  that  of  higher  organisms,  where  contact 
with  the  substratum  is  necessary  in  order  that  progression  may  occur, 
though  all  the  movements  concerned  in  locomotion  may  be  performed 
without  such  contact. 

We  are  compelled  to  conclude,  therefore,  that  in  the  advancing  end  of 
an  Amoeba  or  the  projecting  pseudopodium  there  is  an  active  move- 
ment of  the  protoplasm,  of  a  sort  which  has  not  been  physically 
explained.  This  involves  the  general  conclusion  that  no  physical 
explanation  is  at  present  possible  of  the  locomotion  and  projection  of 
pseudopodia  in  Amoeba. 

To  account  for  the  contraction  of  the  posterior  part  of  the  body,  on 
the  other  hand,  possibly  the  properties  common  to  Amoeba  with  other 
fluids  are  sufficient.  If  surface  tension  may  be  considered  the  cause  of 
the  contraction  of  the  posterior  part  of  the  body,  it  is  notable  that  it 
acts  as  a  constant  factor,  tending  always  to  decrease  the  surface  as  much 
as  possible,  not  as  a  variable  factor.  In  other  words,  there  is  no  indi- 
cation that  local  increase  or  decrease  in  surface  tension  (see  note,  p. 
325)  plays  any  part  in  the  production  of  the  movements,  as  is  main- 
tained in  the  prevailing  theories.  The  part  played  by  surface  tension 
is  thus  a  ver}'  subordinate  one. 

EXPERIMENTAL  IMITATION  OF  MOVEMENTS  DUE  TO  LOCAL  CON- 
TRACTIONS OF  THE  ECTOSARC,  AND  OF  THE  ROUGHENING  OF 
THE  ECTOSARC  IN  CONTRACTION. 

Besides  the  sending  out  of  pseudopodia,  there  are  certain  other  phe- 
nomena in  the  movements  of  Amoeba  for  which  we  lack,  so  far  as  I  am 
aware,  any  attempt  at  a  physical  explanation.  These  are  the  swinging 
movements,  vibrations,  and  local  contractions  of  pseudopodia,  described 
on  pages  177-179?  and  the  roughening  of  the  ectosarc  in  the  contraction 
of  pseudopodia  or  other  parts  of  the  body  (p.  16S). 

These  phenomena  are  in  certain  details  so  similar  to  some  that  I 
have  observed  in  inorganic  fluids  that  I  believe  it  worth  while  to 
analyze  the  latter ;  possibly  they  give  an  indication  of  the  direction  in 
which  an  explanation  of  the  phenomena  in  Amoeba  above  mentioned 
may  lie.* 

*In  view  of  the  repeated  failures  of  physical  explanations  in  attempting  to 
account  for  vital  phenomena,  one  does  not  approach  a  new  attempt  of  this  sort 
with  great  confidence.  Yet  it  is  desirable  that  any  possibility  of  this  kind  should 
be  worked  out  and  submitted  to  criticism,  in  order  that  its  truth  or  lack  of  truth 
may  be  demonstrated. 


2l6  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Swinging  or  bending  movements  take  place  with  special  frequency 
while  the  pseudopodia  are  withdrawing ;  in  some  Amoebse  such  move- 
ments are  an  almost  constant  accompaniment  of  withdrawal.  As  it  is 
withdrawn  the  pseudopodium  becomes  roughened  or  warty  on  its  sur- 
face, as  we  have  seen,  and  at  the  same  time  bends  to  one  side  or  the 
other,  or  swings  back  and  forth.  The  impression  given  is  that  the 
outer  layer  of  the  pseudopodium  has  become  partially  solid.  In  with- 
drawing, the  solid  substance  seems  to  melt  gradually  away,  in  a  some- 
what irregular  manner,  so  as  to  leave  solid  masses  connected  by  liquid 
protoplasm,  the  projecting  solid  masses  forming  the  wart-like  roughen- 
ings  of  the  surface.  When  this  melting  away  occurs  more  strongly  on 
one  side,  the  pseudopodium  bends  at  that  point,  toward  the  side  which 
has  apparently  become  more  fluid. 

We  have  in  such  a  case,  if  appearances  may  be  trusted,  a  mass  com- 
posed partly  of  solid,  partly  of  fluid.  While  it  is  usually  admitted  that 
parts  of  the  protoplasm  may  become  solid  at  times,  little  attempt  has 
been  made  to  understand  protoplasmic  movements  by  studying  the 
physics  of  such  mixtures  of  solids  and  fluids.*  In  certain  experiments 
with  inorganic  mixtures  of  this  kind,  in  which  movements  were  pro- 
duced that  resembled  those  just  referred  to  in  Amoeba,  the  writer 
became  convinced  of  the  possible  importance  of  the  physics  of  such 
mixtures  for  the  understanding  of  protoplasmic  activities. 

The  experiments  in  question  were  concerned  with  the  movements 
under  the  action  of  surface  tension  of  oil  drops  to  which  soot  had  been 
added  for  the  purpose  of  rendering  the  currents  visible.  When  a  large 
quantity  of  soot  was  added,  the  drops  became  somewhat  stiffened,  and 
now  showed  to  a  marked  degree  a  mingling  of  the  characteristic  proper- 
ties of  fluids  and  solids. 

In  one  set  of  experiments  clove  oil  was  thus  mixed  with  soot  and 
introduced  as  drops  into  a  mixture  of  three  parts  glycerine  and  one  part 
95  per  cent  alcohol.  The  drops  move  about,  as  a  result  of  local 
decrease  in  surface  tension,  in  the  same  manner  as  the  olive-oil  emul- 
sion in  Butschli's  celebrated  experiments.  Much  of  the  soot  collects 
next  to  the  surface  of  the  drop,  and  becomes  massed  in  certain  regions, 
as  a  result  of  the  currents,  covering  these  regions  with  a  sort  of  crust, 
this  crust  being  formed  of  separate  solid  particles.  The  particles  are 
crowded  together  as  closely  as  possible,  owing  to  the  surface  tension  of 
the  fluid  in  which  they  are  floating.f  If  the  particles  are  not  too  minute 
they  may  project  above  the  surface  of  the  drop,  giving  it  a  rough  appear- 


♦  Some  of  the  experiments  of  Rhumbler  (1898,  1902)  deal  with  such  mixtures, 
though  not  with  a  view  to  an  understanding  of  the  movements,  but  of  certain 
other  processes. 

t  According  to  the  principles  set  forth  b_y  Rhumbler,  1898,  p.  332. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMOEBA.  21 7 

ance,  similar  to  that  of  the  withdrawing  pseudopodium  of  Amoeba. 
Such  parts  of  drops  or  whole  drops,  so  covered,  show  peculiar  proper- 
ties. The  form  may  be  changed  by  lowering  the  surface  tension  locally 
or  by  mechanical  action  from  outside,  exactly  as  in  a  fluid,  but  there 
is  an  inclination  to  hold  a  form  once  received.  The  tendency  to  take 
the  spherical  form  is  still  somewhat  marked,  and  if  the  irregular  drop 
is  strongly  disturbed  it  frequently  slowly  becomes  spherical.  On  the 
other  hand,  if  not  strongly  disturbed,  it  may  retain  almost  any  form 
impressed  upon  it — cylindrical,  flattened,  irregular,  or  with  long,  slender 
projections.  In  this  power  of  receiving  and  retaining  an  irregular  form, 
yet  with  a  tendency  to  become  spherical,  these  drops,  of  course,  resem- 
ble Amoeba.  These  properties  vary  with  the  amount  of  soot  present  in 
the  oil ;  if  this  is  less,  the  drops  slowly  return  to  the  spherical  shape 
when  deformed  ;  if  greater,  they  retain  the  irregular  shape  indefinitely. 
Such  irregular  masses  nevertheless  flow  together  if  brought  in  contact, 
will  quickly  gather  together  into  a  close  mass  if  strongly  deformed, 
and  in  many  other  ways  they  show  the  characteristics  of  fluids. 

The  reason  for  their  tendency  to  retain  irregular  forms  is  obvious. 
The  surface  is  covered  with  small  solid  particles  that  are  in  contact. 
The  projection  of  these  particles  above  the  surface  may  cause  a  rough- 
ening of  the  surface.  Any  change  of  form,  such  as  surface  tension 
would  produce,  causes  much  friction  between  these  particles.  The 
form  taken  is,  then,  a  resultant  of  the  action  of  surface  tension  and  the 
resistance  of  these  particles  to  movements.*  Similar  forms  are  pro- 
ducible by  mixing  soot  with  bone  oil  and  studying  drops  of  the  mixture 
in  a  vessel  of  glycerine. 

For  our  purpose  the  phenomena  which  occur  when  the  soot  particles 
are  unequally  distributed  are  of  special  interest.  Consider  an  elon- 
gated projection,  as  in  Fig.  78,  A,  with  the  surface  entirely  covered 
with  closely  crowded  soot  particles  except  in  a  certain  region,  x-y^  on 
one  side.  In  this  region  x-y  surface  tension  will  have  free  play,  tend- 
ing to  draw  the  points  x  and  y  together,  while  elsewhere  the  tendency 
to  contraction  will  be  resisted  by  the  friction  of  the  particles.  The 
result  is  that  the  points  x-y  are  drawn  together,  and  the  projection 
bends  toward  that  side.  Since  this  bending  does  not  tend  to  crowd 
the  particles  on  other  parts  of  the  surface  closer  together  they  do  not 
resist  it. 

In  the  oil  drops  mixed  with  soot  the  bending  of  projections  In  the 
manner  described  is  often  to  be  observed  under  the  appropriate  condi- 
tions.    They  should  be  compared  with  the  bending  of  pseudopodia  as 


*  Similar  forms  of  fluids  have  been  produced  by  Rhumbler  in  a  parallel  man- 
ner in  his  imitations  of  the  formation  of  Difflugia  shells  (1898,  p.  287)  and  of 
the  shapes  of  the  shells  of  Foraminifera  (1902,  p.  265). 


3l8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

described  for  Amoeba  (p.  177,  and  Fig.  62,  «) .  The  chief  experimental 
difficulty  in  producing  such  bending  is  to  arrange  the  conditions  in 
such  a  way  that  there  is  less  soot  on  one  side  of  a  projection  than  on 
the  other.  This  occurs  somewhat  frequently  when  two  irregular  drops 
are  allowed  to  fuse,  or  when  a  drop  is  mechanically  deformed  with  a 
rod,  as  described  in  the  next  paragraph.  One  can  sometimes  bring  it 
about  by  placing  with  the  capillary  pipette  a  minute  drop  of  oil  on  one 
side  of  a  projection,  though  this  method  is  not  as  a  rule  very  effective. 
'»  Such  drops  may  also  show  another  prop- 

,,  erty  in  common  with  Amoeba,  namely, 
elasticity  of  form,  or  a  phenomenon  pro- 
ducing similar  results.  Consider  a  curved 
projection,  as  in  Fig.  78,  B.  It  is  com- 
pletely  covered  with  soot  particles  and  re- 
tains its  form  in  vi  rtue  of  their  resistance  to  a 
change  in  position.  Now,  suppose  we  forcibly  straighten  out  the  pro- 
section  by  pushing  it  to  one  side  with  a  rod.  By  so  doing  the  side  a-6 
is  lengthened  ;  the  soot  particles  on  this  side  are,  therefore,  separated, 
leaving  certain  areas  of  free  fluid  surface.  When  the  projection  is 
released,  surface  tension  can  act  on  these  areas,  and  the  projection  is 
drawn  back  at  once  to  its  original  form.  I  have  often  observed  such 
immediate  returns  to  the  original  form  after  bending  a  projection  of 
one  of  the  oil  drops. 

In  Amoeba  we  have  exactly  the  conditions  most  favorable  for  the 
production  of  movements  of  this  sort,  and  we  actually  find  numerous 
movements  of  just  this  character.  It  is  generally  admitted  that  the 
outer  layer  becomes  partially  solidified  ;  as  a  pseudopodium  is  with- 
drawn the  solid  portions  evidently  become  liquefied  in  an  irregular 
way,  some  of  them  projecting  above  the  surface  and  making  it  rough. 
If  the  liquid  substance  produced  shows  surface  tension,  the  movements 
described  must  follow  in  the  manner  set  forth  above.  It  seems  possible 
that  many  of  the  observed  movements  are  thus  produced  by  local  lique- 
faction, with  the  intervention  of  surface  tension,  in  the  liquefied  area. 
In  view  of  the  apparently  unlimited  possibilities  of  partial  solidifica- 
tion and  liquefaction  in  the  protoplasmic  body,  with  the  resulting  varied 
action  of  surface  tension,  shall  we  not  go  a  step  farther  and  inquire 
whether  there  may  not  be  an  outlook  for  an  explanation  of  vibratory 
movements,  such  as  we  find  in  flagella,  along  this  line.''  In  an  elon- 
gated structure  like  a  flagellum,  a  limited  liquefaction  of  one  side  would 
result  in  a  bending  toward  this  side.  By  regular  alternation  of  lique- 
factions in  different  regions,  a  regular  vibration  could  be  produced. 
The  chief  difficulty  in  the  way  of  such  a  theory  would  seem  to  lie  in 
*FiG.  78. — Diagrams  illustrating  phenomena  in  mixtures  of  oil  and  soot. 


THE    MOVEMENTS    AND    IlEACTlOXS   OF    AMCEBA,  2X9 

the  restoration  of  the  original  length  in  a  given  side  after  liquefaction 
and  consequent  contraction  had  occurred.  This  could,  perhaps,  be 
brought  about  by  an  elastic  rod  in  the  axis  of  the  structure,  such  as 
many  cilia  and  flagella  are  known  to  possess. 

The  above  is  merely  a  suggestion  made  tentatively  ;  its  justification 
as  a  suggestion  lies  in  the  following  facts:  (i)  The  swinging  move- 
ment of  pseudopodia  in  Amoeba  in  some  cases  strikingly  resembles 
movements  of  the  character  above  set  forth  in  inorganic  fluids,  and 
precisely  the  conditions  for  such  movements  are  present  in  Amoeba ; 
(2)  Swinging  movements  of  pseudopodia  seem  to  grade  almost  insen- 
sibly into  the  vibratory  movements  of  flagella. 

DIRECT     OR     INDIRECT     ACTION     OF    EXTERXAL    AGENTS     IN 
MODIFYING    THE    MOVEMENTS. 

Is  the  effect  of  external  agents  in  modifying  the  movements  of  Amoeba 
due  to  the  direct  physical  action  of  the  agent  on  that  part  of  the  fluid 
substance  with  which  it  comes  in  contact?  Or  is  its  action  indirect, 
in  that  it  serves  merely  as  a  stimulus  to  certain  internal  changes,  the 
latter  bringing  about  the  modifications  in  the  behavior?  Both  views 
find  adherents.  The  difference  between  them  is  fundamental,  for  they 
lead  to  essentially  different  conceptions  as  to  the  nature  of  behavior  in 
these  lower  organisms. 

In  higher  animals  we  know  that  the  movements  and  changes  of 
movement  are  not  produced  in  a  direct  way,  but  the  effect  of  external 
agents  is  to  cause  internal  alterations  which  result  in  changes  of  move- 
ment. It  is  not,  therefore,  possible  to  predict  the  movements  of  the 
organism  from  a  knowledge  of  the  direct  physical  changes  produced  in 
its  substance  by  the  agent  in  question.  If  the  theory  of  direct  action  is 
correct  for  Amoeba,  we  have  in  these  animals  a  condition  of  affairs  incom- 
parably simpler,  for  here  we  can  resolve  the  behavior  directly  into  its 
physical  factors.  If,  on  the  other  hand,  the  theory  of  indirect  action  is 
correct,  then  there  appears  to  be  nothing  fundamentally  different  in 
principle  between  the  behavior  of  Amoeba  and  that  of  higher  organisms. 

How  the  form  and  movement  of  a  fluid  mass  might  be  determined 
by  the  direct  action  of  external  agents  on  its  surface  may  be  simply 
illustrated  by  certain  experiments  which  I  have  described  elsewhere 
(Jennings,  1902).  A  mixture  of  2  parts  glycerine  and  i  part  95  per 
cent  alcohol  is  placed  on  a  slide  and  covered  with  a  cover  glass  sup- 
ported by  glass  rods.  Into  this  is  introduced  with  a  capillary  pipette 
a  drop  of  clove  oil.  The  clove-oil  drop,  at  first  circular  in  form,  soon 
changes  shape,  shows  internal  currents,  sends  out  projections  in  various 
directions,  moves  about  from  place  to  place,  and  may  divide  into  two 
drops.  The  alcohol,  not  being  uniformly  distributed  throughout  the 
glycerine,  acts  more  strongly  on  some  parts  of  the  clove-oil  drop  than 


220  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

on  others,  thus  lowering  the  surface  tension  in  the  region  acted  upon. 
Thereupon  the  drop  sends  out  a  projection  on  the  side  affected,  and  may 
follow  this  up  by  moving  in  that  direction.  We  may  cause  the  drop  to 
send  out  projections  and  move  in  a  certain  direction  by  placing  a 
minute  drop  of  alcohol  near  one  side,  or  by  heating  one  side ;  move- 
ment takes  place  toward  the  side  affected.  These  agents  act  directly 
on  the  surface  of  the  drop,  lowering  the  tension  ;  the  movements  are  a 
direct  consequence  of  this  change.  Parallel  phenomena  maybe  pro- 
duced, as  Bernstein  (1900)  has  shown,  with  a  drop  of  quicksilver.  If 
such  a  drop  is  placed  in  10  per  cent  nitric  acid,  in  which  bichromate 
of  potash  has  been  dissolved,  the  drop  changes  form  and  moves  about. 
If  we  place  near  such  a  drop,  in  vessel  of  10  per  cent  nitric  acid,  a 
crystal  of  potassium  bichromate,  the  mercury  drop  moves  rapidly  over 
to  the  crystal.  Here,  again,  the  chemical  acts  directly  on  the  mercury, 
lowering  the  surface  tension  at  the  region  where  it  comes  in  contact 
with  it,  thus  producing  the  movement. 

Certain  authors  have  held  that  the  movements  of  Amoeba  are  pro- 
duced in  this  way  by  the  direct  action  of  external  agents  decreasing 
or  increasing  the  surface  tension  of  certain  parts  of  the  fluid  mass.  As 
an  example  of  the  theory  of  direct  action  of  external  agents  in  control- 
ling the  behavior,  we  may  take  the  view  of  the  reaction  of  Amceba  to 
chemicals  recently  given  by  Rhumbler  (1902,  p.  384).  According  to 
Rhumbler,  it  is  evident  that  when  an  Amoeba  moves  toward  or  away 
from  a  certain  chemical,  the  side  directed  toward  the  chemical  has,  in 
the  first  case,  a  lessened  surface  tension,  in  the  second  case  an  increased 
surface  tension,  as  compared  with  the  remainder  of  the  body. 

The  necessary  differences  of  tension  on  the  positive  and  negative  sides  may  be 
easily  understood  from  our  present  standpoint,  by  holding  that  a  positively 
acting  chemical  decreases  the  surface  tension  both  in  the  living  alveolar  system 
of  the  cell  and  especially  on  the  cell  surface,  upon  which  it  must  work  most 
strongly;  that  a  negatively  acting  chemical,  on  the  other  hand,  produces  an 
increase  of  surface  tension  in  the  alveoli  of  the  cell,  and  especially,  again,  on  the 
cell  surface;  this  increase  is  the  greater,  and  from  a  physical  standpoint  must  be 
the  greater,  the  more  the  molecules  of  the  chemical  affect  or  modify  the  tension 
of  the  different  cell  alveoli  or  different  parts  of  the  cell  surface  (/.  c,  p.  384). 

The  explanation  of  thermotaxis  and  electrotaxis  would  be,  according 
to  Rhumbler,  "exactly  the  same  as  for  chemotaxis"  (/.  c,  p.  385)  ; 
thus  also  as  a  result  of  the  direct  action  of  external  agents.  A  fuller 
explanation  of  the  "  tropisms  "  on  this  basis  is  given  by  Rhumbler  in 
an  earlier  paper  (1898,  pp.  183,  188).* 

*  Rhumbler  emphasizes  in  the  paper  just  cited  (1898,  p.  184)  the  importance 
of  "  inner  disposition  "  in  deciding  what  effect  shall  be  produced  by  external 
agents,  but  in  the  tropisms,  at  least,  he  considers  the  action  of  the  external  agent 
to  be  direct,  the  inner  disposition  deciding  merely  whether  the  substance  of  the 
Amceba  is  of  such  a  character  as  to  admit  of  the  production  of  a  given  definite 
change  in  surface  tension  by  the  outer  agent. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  221 

Based  similarly  on  a  direct  action  of  external  agents  is  the  theory  of 
amoeboid  movements  proposed  by  Verworn  in  1891,  and  extended  in 
his  paper  on  Die  Bewegung  der  lebendigen  Substanz  (1892)  and  in 
the  Allgetneine  Physiologie.  In  its  original  form  Verworn's  theory 
considers  the  movements  and  changes  of  form  to  be  brought  about 
directly  through  chemical  attraction  (Verworn,  1891,  p.  105),  but  in 
later  publications  (1892,  1895)  the  effect  of  the  chemical  is  considered, 
as  in  Rhumbler's  theory,  to  be  that  of  increasing  or  decreasing  the 
surface  tension. 

Thus  it  is  evident  that  it  must  be  the  chemical  affinity  of  certain  parts  of  the 
protoplasm  for  oxygen  that  decreases  the  surface  tension  in  definite  regions  and 
thus  leads  to  the  formation  of  pseudopodia.  But  it  will  be  possible  for  the  same 
effect  to  be  produced  by  other  substances  of  the  surrounding  medium,  if  they 
have  chemical  affinity  for  certain  components  of  the  protoplasm.  In  the  case 
where  the  substance  acts  from  one  side,  this  principle  must  lead  to  positive 
chemotropism.     (Vervvrorn,  1895,  p.  545.) 

It  is  evident  that  the  method  of  movement  of  Amoeba,  as  described 
in  this  paper,  has  an  immediate  bearing  on  the  question  of  direct  or 
indirect  action  of  external  agents.  If  the  action  of  an  external  agent 
is  to  increase  or  decrease  directly  the  surface  tension,  as  set  forth  by 
Rhumbler  and  Verworn,  this  effect  must  be  shown  in  the  characteris- 
tic currents  which  appear  in  any  fluid  when  the  surface  tension  is  thus 
locally  changed.  In  the  case  of  negative  chemotaxis  we  should  have 
an  axial  current  away  from  the  side  affected,  with  surface  currents 
toward  the  chemical,  as  indicated  in  the  figure  given  by  Rhumbler 
(1898,  p.  188).  In  positive  chemotaxis  both  sets  of  currents  should  be 
the  reverse  of  that  just  indicated. 

In  the  account  of  the  movements  set  forth  by  Biitschli  and  Rhumbler, 
the  currents  agreed  with  the  scheme  for  direct  action  above  set  forth. 
But  this  account  of  the  movements  was  erroneous,  as  we  have  seen. 
The  internal  currents  and  the  surface  currents  are  forward,  away  from 
the  region  stimulated,  in  a  negative  reaction  ;  toward  the  region  stim- 
ulated in  a  positive  reaction ;  the  movement  is  of  a  rolling  character. 
There  is  thus  no  evidence  that  the  action  of  the  stimulus  is  to  cause  a 
change  in  the  surface  tension  of  the  parts  directly  affected  ;  on  the  con- 
trary, the  direction  of  the  currents  is  quite  inconsistent  with  this  view.* 
We  must  conclude,  then,  that  the  theory  of  the  direct  action  of  exter- 
nal agents  in  causing  or  changing  the  movements  of  Amoeba  is  nega- 
tived by  the  character  of  the  movements  produced  ;  these  are  not  such  as 
would  follow  from  the  direct  physical  action  of  the  agents  in  question. 

*  A  description  of  the  forward  surface  currents  in  negative  chemotaxis  is  given 
on  p.  143;  in  the  reaction  to  a  mechanical  stimulus  on  p.  185;  to  the  electrical 
stimulus  on  p.  192  ;  in  a  positive  food  reaction  (chemical  and  mechanical  stimuli  ?) 
on  p.  198. 


222  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

There  is  much  indirect  evidence  that  points  in  the  same  direction, 
particularly  in  the  fact  that  the  activities  of  the  animal  may  remain  con- 
stant while  the  environment  is  continually  chanj^^ing.  Some  of  these 
lines  of  evidence  are  summarized  by  Rhumbler  (1898,  p.  185).  They 
still  leave  open  the  possibility  that  when  the  environment  does  modify 
the  movements  its  action  is  direct.  But  even  this  is  shown  to  be 
excluded  by  the  nature  of  the  currents  produced,  as  described  above. 

The  currents  as  they  actually  occur  in  the  movements  are  equally 
opposed  to  certain  theories  of  the  indirect  action  of  stimuli.  Bernstein 
(1900),  Jensen  (1901),  and  others,  have  expressed  the  opinion  that  the 
effect  of  stimuli  is  to  change  the  surface  tension,  but  that  this  effect  is 
not  due  to  the  direct  physical  action  of  the  agent  on  the  protoplasm, 
but  rather  to  some  change  in  the  internal  physiological  processes  of  the 
cell  produced  by  the  agent  acting  as  a  stimulus.  Jensen  (1901,  1902) 
has  developed  this  view  into  a  detailed  theory,  according  to  which 
stimuli  that  increase  the  normal  assimilatory  processes  of  the  cell  lead 
to  a  reduction  of  surface  tension,  and  hence  to  expansion  and  move- 
ment toward  the  agent  in  question,  while  stimuli  that  increase  the 
dissimilatory  processes  have  the  opposite  effect. 

The  currents  in  the  moving  Amoeba  lend  no  support  to  this  view. 
There  is  no  evidence  in  the  movement  that  the  effect  of  a  stimulus  is  to 
alter  the  surface  tension  in  any  way.  In  view  of  the  facts  given  in  the 
body  of  this  paper  as  to  the  nature  of  the  movements,  we  are  forced  to 
give  up  the  idea  that  the  effect  of  stimuli  is  to  modify  the  tension*  of 
the  surface  of  the  protoplasmic  mass,  either  directly  or  indirectly. 
Alterations  in  the  tension  of  the  surface  can  no  longer  be  considered 
the  prime  factor  in  the  behavior  of  Amoeba. 

DIRECT    OR    INDIRECT    ACTION    IN   THE    TAKING    OF    FOOD. 

Rhumbler,  in  his  most  interesting  and  suggestive  paper  (189S),  has 
attempted  to  give  a  physical  analysis  of  food-taking  and  the  choice  of 
food  in  Amoeba.  According  to  Rhumbler,  the  taking  of  food  is  due 
to  adhesion  between  the  protoplasm  and  the  food  substance,  and  may 
be  compared  with  the  pulling  inward  of  a  splinter  of  wood  by  a  drop  of 
water,  or  of  a  bit  of  shellac  by  a  drop  of  chloroform.  The  selection  of 
food  is  explained  as  due  to  the  fact  that  the  protoplasm,  as  might  be 
expected  from  physical  considerations,  tends  to  adhere  to  some  sub- 
stances and  not  to  others.  Parallel  phenomena  are  shown,  in  a  most 
ingenious  experiment,  to  be  demonstrable  for  the  chloroform  drop 
(/.  c,  p.  248).  It  takes  in  certain  substances,  while  others  are  refused 
or  thrown  out  if  introduced. 


♦See  note,  p.  235. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  223 

This  theory  is  a  most  attractive  one,  and  seems  a  priori  probable.* 
It  is  conceivable  that  there  may  be,  or  may  have  been,  organisms  where 
it  is  applicable  throughout.  But  an  objective  study  of  the  behavior  of 
Amoeba  show^s  that  it  gives  by  no  means  an  adequate  explanation  of 
food-taking  in  this  animal.  As  I  have  shown  in  the  descriptive  por- 
tion, in  Ammba  proteus  and  A.  angulata  the  food  in  most  cases  is  far 
from  adhering  to  the  protoplasm  ;  on  the  contrary,  it  rolls  away  when 
the  Amoeba  comes  in  contact  with  it,  and  it  is  often  only  as  a  result  of 
long-continued  effort  that  the  animal  succeeds  in  ingesting  it.  The 
first  act  in  ingestion  consists  in  sending  out  pseudopodia  on  each  side  of 
the  mass  to  overcome  the  mechanical  difficulty  resulting  from  the  fact 
that  the  body  does  ;?d?/ adhere  to  the  protoplasm,  but  tends  to  roll  away. 

Further,  a  quantity  of  water  is  usually,  or  frequently,  taken  in  with 
the  food,  and  the  latter  floats  about  in  a  cavity  after  it  is  ingested,  show- 
ing no  tendency  to  adhere  to  the  protoplasm  (see  Leidy,  1879,  numer- 
ous figures  of  food  vacuoles,  etc.,  and  Le  Dantec,  1S94).  A  similar 
condition  of  affairs  is  shown  in  the  account  of  the  feeding  of  one 
Amoeba  on  another,  given  on  page  201  of  the  present  paper.  Here  the 
prey  does  not  adhere  to  the  protoplasm  of  its  captor,  but  moves  about 
within  the  latter  and  escapes  repeatedly. 

Thus,  in  these  species,  the  taking  of  food  and  the  choice  of  food  can- 
not be  explained  by  the  adherence  of  the  protoplasm  to  the  food  sub- 
stance, for  the  lack  of  such  adherence  is  strikingly  evident. 

Rhumbler's  studies  of  food  taking  were  made  chiefly  on  Animba 
verrucosa.  In  this  species  and  its  close  relatives  there  is  much  more 
tendency  for  foreign  objects  to  cling  to  the  surface  than  in  the  other 
species.  But  this  adhesiveness  applies  to  other  objects  as  well  as  to 
food.  It  is  of  special  aid,  as  we  have  seen,  in  tracing  surface  move- 
ments (p.  140).  Particles  of  soot  and  various  other  indifierent  bodies 
stick  to  the  surface,  rendering  its  movements  apparent.  Not  all  such 
adhering  bodies  are  taken  into  the  interior,  so  that  the  ingestion 
involves  an  additional  reaction,  and  is  not  fully  accounted  for  by  the 
adhesion  even  in  these  species. 

Rhumbler  has  given  an  ingenious  physical  analysis  of  the  rolling  up 
and  taking  in  of  filaments  of  Oscillaria  by  Amoeba  verrucosa^  and  has 
illustrated  the  process  as  he  conceives  it  to  occur  by  a  very  striking 
experiment  (1S98,  p.  230).  A  chloroform  drop  brought  in  contact 
with  the  middle  of  a  filament  of  shellac  rolls  the  filament  together  and 
encloses  it.  Rhumbler  conceives  the  forces  at  work  in  rolling  up  the 
filament  to  be  essentially  the  same  in  the  chloroform  drop  and  in  the 
Amoeba.     In  both  cases,  according  to  Rhumbler,  the  surface  tension  of 

♦See  Jennings,  1902,  where  I  adopted  this  view  before  having  investigated  for 
nnyself  the  behavior  of  Amoeba. 


224  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  drop  pulls  on  the  filament,  tending  to  force  it  inward  from  both 
directions.  That  part  of  the  filament  within  the  drop  becomes  softened 
by  the  action  of  the  fluid ;  it,  therefore,  yields  to  the  thrust  from  both 
directions,  and  bends,  permitting  more  of  the  filament  to  be  brought 
into  the  drop  by  the  action  of  surface  tension.  (For  full  explanation, 
see  the  original.) 

It  is  necessary  to  point  out  that  the  explanation  of  the  rolling  up  of 
the  shellac  filament  given  by  Rhumbler  is  erroneous.  The  surface 
tension  of  the  drop,  with  its  inward  thrust,  has  nothing  to  do  with  the 
process,  for  the  filament  is  rolled  up  in  exactly  the  same  manner  when 
it  is  completely  submerged  in  a  large  vessel  of  chloroform,  so  that  it  is 
not  in  contact  with  the  surface  film  at  all.  The  rolling  up  is  evidently 
due  in  some  way  to  the  strains  within  the  shellac  filament,  produced 
when  it  was  drawn  out,  and  to  the  adhesiveness  of  its  surface  when 
acted  upon  by  the  chloroform.  The  process  thus  loses  all  similarity 
to  the  rolling  up  of  the  alga  filament  by  Amoeba.  The  coil  formed  is 
just  as  small  and  close,  and  the  filament  remains  a  filament  just  as  long 
when  the  experiment  is  tried  in  a  large  vessel  of  chloroform  as  when 
only  a  drop  is  used,  as  in  Rhumbler's  experiments. 

Rhumbler's  explanation  of  the  way  in  which  Amoeba  rolls  up  the 
Oscillaria  filament  may,  of  course,  still  be  correct,  though  the  physical 
experiment  by  which  he  attempted  to  illustrate  it  has  nothing  to  do 
with  the  matter.  There  are  certain  points  in  his  description  of  the  pro- 
cess as  it  occurs  in  Amoeba,  however,  that  might  easily  be  interpreted 
in  another  manner.  Such  a  bending  over  of  the  pseudopodium  as  is 
shown  in  Rhumbler's  Fig.  58  (/.  c,  p.  233)  is  not  called  for  by  the 
surface-tension  theor)-.  Rhumbler  holds  that  this  bending  of  the  pseu- 
dopodium is  passive,  and  due  to  the  bending  of  the  filament  within  the 
body  (/.<:.,  p.  233).  In  view  of  what  we  have  shown  above  (pp.  177-179) 
as  to  the  power  of  active  bending  in  the  pseudopodia,  and  as  to  active 
contractions  of  parts  of  the  ectosarc  in  this  same  species  (pp.  179,  iSo), 
one  might  be  inclined  to  believe  rather  that  this  bending  of  the  pseu- 
dopodium is  active  and  plays  an  important  part  in  bringing  the  fila- 
ment into  the  body.  Rhumbler's  figures  (Fig.  50)  would  support  this 
view  fully  as  strongly  as  his  own  theory,  though  this  would,  of  course, 
not  give  us  a  simple  physical  explanation  of  the  ingestion  of  the  filament. 

Altogether,  we  must  conclude  that  adhesion  between  the  protoplasm 
and  the  food  substance  cannot  by  any  means  give  us  a  general  explana- 
tion of  food-taking  in  Amoeba.  In  some  cases  the  ingestion  of  food 
is  aided  by  such  adhesion,  but  in  other  cases  the  adhesion  is  conspicu- 
ously absent.* 

*  For  further  confirmation  of  last  stated  fact,  see  paper  of  Le  Dantec  ('1894). 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  225 

GENERAL   CONCLUSION. 

Putting  all  our  results  together,  we  must  conclude  that  the  move- 
ments and  reactions  of  Amoeba  have  as  yet  by  no  means  been  resolved 
into  their  physical  components.  Amoeba  is  a  drop  of  fluid  which 
moves  in  its  usual  locomotion  in  much  the  same  way  as  inorganic  drops 
move  under  the  influence  of  similarly  directed  forces.  But  what  these 
forces  are  is  by  no  means  clear.  When  we  take  into  considera- 
tion the  currents  as  they  actually  exist,  local  decrease  in  surface  tension 
breaks  down  completely  as  an  explanation  for  the  locomotion  and  other 
movements.  The  locomotion  taken  by  itself  might  be  explained  as  due 
to  the  adhesion  of  the  fluid  protoplasm  to  solids,  taken  in  connection 
with  the  surface  tension  of  the  fluid,  but  this  explanation  fails  when  we 
consider  the  formation  of  free  pseudopodia,  and  discover  that  all  the 
processes  concerned  in  locomotion  can  take  place  without  adhesion  to 
the  substratum. 

For  the  reactions  to  stimuli  we  find  a  parallel  condition  of  affairs. 
The  currents  in  the  protoplasm  in  the  positive  and  negative  reactions 
are  not  similar  to  those  produced  in  the  attraction  or  repulsion  of  drops 
of  fluid  by  the  direct  action  of  external  agents.  Therefore  we  cannot 
consider  these  reactions  as  due  to  the  increase  or  decrease  of  surface 
tension*  produced  by  the  direct  (or  even  indirect)  action  of  the  external 
agents.  The  taking  and  choice  of  food  cannot  be  physically  explained 
in  any  general  way  by  the  physical  adherence  of  the  protoplasm  as  a 
substance  to  the  food  as  a  substance,  for  food  is  taken  in  many  cases 
(usually,  in  some  species)  where  it  is  demonstrable  that  no  such 
adherence  exists. 

While  we  must  agree  that  Amoeba,  as  a  drop  of  fluid,  is  a  marvel- 
lously simple  organism,  we  are  compelled,  I  believe,  to  hold  that  it  has 
many  traits  which  are  comparable  to  the  ''reflexes"  or  "habits"  of 
higher  organisms. f     VVe  may,  perhaps,  have  faith  that  such  traits  are 


♦It  should  be  pointed  out  that  this  and  other  statements  concerning  surface 
tension  in  Amoeba  apply  to  the  tension  of  the  actual  body  surface,  comparing 
Amoeba  thus  to  a  drop  of  simple  fluid.  This  is  the  basis  on  which  rest  the  pre- 
vailing theories  that  would  explain  the  movements  of  AmcBba  by  surface  tension. 
It  is  these  theories  which  I  desired  to  test.  There  remains  untouched,  of  course, 
the  possibility  that  the  movements  of  all  sorts  of  protoplasmic  masses  may  be 
explained  by  changes  in  the  surface  tension  of  the  meshes  of  Butschli's  honey- 
comb structure,  in  the  manner  indicated  by  Biitschli  (1892,  p.  208).  But  this  is 
at  present  merely  a  hypothesis,  not  worked  out  and  not  controllable  by  observa- 
tion. To  attempt  to  maintain  it  for  Amoeba  would  be  to  relegate  the  movements 
of  this  animal  to  the  same  obscure  category  as  the  movements  of  cilia  and  of 
muscles,  possibly  a  correct  proceeding,  but  removing  the  matter  at  present  from 
the  field  of  experimental  observation. 

t  See  the  next  division  of  this  paper,  where  this  point  is  developed. 


226  THE  BEHAVIOR    OF    LOWER    ORGANISMS. 

finally  resolvable  into  the  action  of  chemical  and  physical  laws,  but  we 
must  admit  that  we  have  not  arrived  at  this  goal  even  for  the  simpler 
activities  of  Amoeba. 

THE  BEHAVIOR  OF  AMCEBA  FROM  THE  STANDPOINT  OF  THE 
COMPARATIVE  STUDY  OF  ANIMAL  BEHAVIOR. 

HABITS     IN   AMCEBA. 

Although  in  general  Amoeba  has  the  rolling  movement  of  a  drop  of 
fluid,  yet  this  statement  by  no  means  brings  out  all  the  characteristics 
of  the  movement  in  any  given  species  of  Amoeba.  Different  kinds  of 
Amoebae  move  differently,  and  the  differences  are  in  many  cases  not 
such  as  can  be  accounted  for  by  differences  in  the  state  of  aggregation 
of  the  body  substance.  Some  Amoebae,  as  is  well  known,  form  many 
pseudopodia,  others  few  or  none.  Different  Amoebae  have  different 
characteristic  forms  in  locomotion.  But  more  striking  than  these  gen- 
erally recognized  peculiarities  are  certain  others  of  a  more  special  char- 
acter. A  creeping  Amoeba  angulata^  as  we  have  seen  above,  frequently 
pushes  upward  and  forward  at  the  anterior  end  a  short,  acute  pseudo- 
podium,  which  waves  slightly  from  side  to  side  like  an  antenna  (p.  177 
and  Fig.  62,  c).  This  peculiar  habit  is  much  more  pronounced  in 
Amoeba  velata  Parona,  according  to  Penard  (1902).  In  this  animal 
the  free  anterior  pseudopodium  may  extend  for  a  length  greater  than 
the  diameter  of  the  body  ;  Penard  compares  it  directly  to  a  tentacle. 
Some  other  species  of  Amoeba  never  send  forward  such  an  antenna-like 
pseudopodium.  The  great  work  of  Penard  (/.  c.)  contains  innumer- 
able instances  of  such  peculiarities  of  form,  movement,  and  function 
among  the  different  species  of  Amoeba  and  other  Rhizopods  ;  some  of 
them  are  collected  in  that  author's  interesting  section  on  the  pseudo- 
podia (/.  c,  pp.  625-629).  It  is  not  necessary  to  take  these  up  in  detail 
here.  \  The  point  of  interest  is  that  different  sorts  of  Amoebae  have  dif- 
ferent customary  methods  of  action,  such  as  are  commonly  spoken  of 
as  "  habits"*  in  higher  animals,  and  that  these  *'  habits"  are  no  more 
easily  explicable  on  direct  physical  grounds  in  Amoeba  than  in  higher 
animals.  Let  anyone  attempt,  for  example,  to  explain  from  the 
physics  of  viscous  fluids  why  Amoeba  velata  or  A.  angulata  push 
out  an  antenna-like  pseudopodium  at  the  anterior  end  and  wave  it  from 
side  to  side,  while  Amoeba  proteus  and  A,  Umax  do  not. 


*  The  word  habit  is,  of  course,  not  used  here  of  a  method  of  action  acquired 
during  the  life  of  the  individual,  but  merely  of  a  fixed  method  of  behavior.  At 
all  events,  it  is  difficult  to  distinguish  between  these  two  things  where  individual 
organisms,  as  in  Amoeba,  have  lived  as  long  as  the  race. 


THE   MOVEMENTS   AND    REACTIONS    OF   AMCEBA.  227 

CLASSES    OF   STIMULI   TO    WHICH    AMCEBA    REACTS. 

The  simple  naked  mass  of  protoplasm  reacts  to  all  classes  of  stimuli 
to  which  higher  animals  react  (if  we  consider  the  auditory  stimulus 
merely  a  special  case  of  the  mechanical  stimulus).  Mechanical  stimuli, 
chemical  stimuli,  temperature  differences,  light,  and  electricity — all 
control  the  direction  of  movement,  as  they  do  in  higher  animals. 

TYPES    OF    REACTION. 

Amoeba  has  two  chief  types  of  reaction,  by  one  or  the  other  of  which 
it  responds  to  most  stimuli.  These  we  may  call  the  positive  and  the 
negative  reactions.  As  a  third  type  we  must  distinguish  the  food 
reaction,  which  cannot  be  brought  completely  under  either  of  the  two 
chief  types  of  reaction  above  mentioned. 

(i)  The  positive  reaction  consists  in  pushing  out  the  body  substance 
toward  the  source  of  stimulus  and  rolling  in  that  direction. 

(2)  The  negative  reaction  consists  in  withdrawal  of  body  substance 
and  rolling  in  some  other  direction — not  necessarily  in  the  opposite 
direction. 

(3)  The  food  reaction  is  not  sharply  definable.  Its  most  character- 
istic features  consist  in  the  hollowing  out  of  the  anterior  end  and  in 
the  pushing  out  of  pseudopodia  at  each  side  of  and  over  the  food  body. 
It  involves  also  the  positive  reaction  above  characterized. 

RELATION    OF    THE     DIFFERENT    REACTIONS    TO    DIFFERENT    STIMULI  ; 
ADAPTATION    IN    THE    BEHAVIOR    OF    AMCEBA. 

(a)  The  positive  reaction  is  known  to  be  produced  by  weak  mechanical 
stimuli ;  it  is  probably  produced  also  by  weak  chemical  stimuli  (in  the 
reactions  to  food,  pp.  193-202).  The  positive  reaction  to  weak  mechan- 
ical stimuli  serves  the  purpose  of  bringing  the  floating  animal  to  a  sur- 
face on  which  it  can  creep.  The  positive  reaction  to  food  substances 
(mechanical  and  chemical  stimuli),  of  course,  serves  to  obtain  food. 
The  positive  reaction  is  thus,  as  a  rule,  performed  under  such  circum- 
stances as  to  be  beneficial  to  the  organism  ;  z.  e.,  it  is  directly  adaptive. 

(6)  The  negative  reaction  is  produced  by  powerful  stimuli  of  all 
sorts.  Such  powerful  stimuli  are,  as  a  rule,  injurious,  and  the  nega- 
tive reaction  tends  to  remove  the  Amoeba  from  their  action  ;  it  is,  there- 
fore, directly  adaptive.  This  is  true  of  the  negative  reaction  to  light 
as  well  as  to  other  stimuli,  for  light  is  known  to  interfere  with  the  activi- 
ties of  Amoeba.  \The  reaction  to  the  electric  current  is  of  exactly  the 
character  that  would  be  produced  by  a  strong  stimulus  on  the  anode 
side,  but  owing  to  the  peculiarity  of  the  current  the  reaction  does  not 
assist  the  Amoeba  to  escape.  The  reaction  to  the  electric  current  can 
not  then  be  considered  adaptive  ;  this  stimulus  forms,  of  course,  no 
part  of  the  normal  environment  of  an  Amoeba., 


22^  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

The  method  by  which,  througfh  the  negative  reaction,  Amoeba  avoids 
an  injurious  agent  is  of  interest.  The  animal  does  not  go  directly  away 
from  the  injurious  agent,  as  by  moving  toward  the  side  opposite  that 
stimulated.  It  moves  in  any  direction  except  toward  the  region  stimu- 
lated. There  is  no  system  of  conduction  such  that  strong  stimulation  in 
a  given  spot  involves  movement  directed  toward  the  opposite  side.  If 
the  movement  in  the  new  direction  induces  a  new  stimulation,  the  direc- 
tion is  again  changed.  This  may  be  continued  until  the  original  direction 
of  movements  is  squarely  reversed.  The  method  is  akin  to  that  of  trial 
and  error  in  higher  organisms  (see  Morgan,  1S94,  pp.  241-242).; 

(c)  The  food  reaction  is  directly  adaptive  in  that  it  procures  food. 
As  a  rule  this  reaction  occurs  only  when  the  source  of  stimulation  is 
fitted  to  serve  as  food.  Empty  diatom  shells,  sand  grains,  debris,  etc., 
are,  as  a  rule,  not  taken  into  the  body,  as  many  observers  have  pointed 
out.  Sometimes  material  is  taken  into  the  body  that  is  not  useful,  as 
is  described  by  Rhumbler  (1898,  p.  236).  In  such  cases  there  is  no 
evidence  of  a  food  reaction  in  the  sense  characterized  above ;  the 
material  is  ingested  accidentally,  as  it  were,  through  its  adherence  to 
the  protoplasm.  The  food  reaction,  as  a  definite  form  of  behavior,  is 
always  adaptive  so  far  as  known. 

(d)  Some  of  the  habits  of  Amoeba,  characterized  above,  are  clearly 
adaptive.  The  use  of  the  antenna-like  pseudopodium  sent  out  by 
Amoeba  velata  and  A,  a7tgulata  is  evident.  Penard  describes  in  detail 
how  Amoeba  velata  uses  it  in  passing  from  one  substratum  to  another. 

The  habit  which  some  Amoebae  have,  when  suspended  freely  in  the 
water,  of  sending  out  pseudopodia  in  all  directions  (p.  181)  is,  of  course, 
useful  in  that  it  increases  the  chances  of  coming  in  contact  with  some 
solid  object,  without  which  the  Amoeba  cannot  move  from  place  to 
place. 

REFLEXES    AND    "  AUTOMATIC    ACTIONS  "    IN   AMCEBA. 

In  the  behavior  of  Amoeba  we  can  distinguish  factors  directly  com- 
parable to  the  reflexes  and  '*  automatic  activities  "  of  higher  organisms. 
The  responses  of  Amoeba  to  stimuli  have  the  nature  of  reflexes  in  the 
fact  that  they  are  not  direct  efl^ects  of  the  physical  action  of  the  stimulus 
(see  p.  219),  but  are  determined  by  the  internal  conditions  of  the 
organism.  They  may  be  called  reflexes,  unless  we  propose,  as  certain 
writers  do,  to  restrict  the  term  reflex  to  processes  involving  difleren- 
tiated  nerves.  The  precise  designation  is  unimportant ;  the  essential 
point  is  that  the  responses  agree  with  the  reflexes  of  higher  animals  in 
being  indirect. 

Ziehen,  in  his  JLeitfaden  der  physiologischen  Psychologie  (sixth 
edition,  p.  10),  defines  as  automatic  acts  "  motor  reactions,  which  do 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  229 

not,  like  the  reflexes,  follow  unchangeably  upon  a  definite  stimulus, 
but  which  are  modified  in  their  course  by  new,  intercurrent  stimuli." 
In  this  sense  Amoeba,  of  course,  shows  automatic  behavior.  Its 
responses  are  by  no  means  unchangeably  fixed  ;  on  the  contrary,  its 
behavior  is  often  modified  by  the  slightest  change  in  the  stimulus  to 
which  it  is  reacting.  For  examples  of  this  see  the  chase  of  one  Amoeba 
by  another  (p.  200),  the  following  of  a  rolling  ball  of  food  (p.  196),  the 
account  of  the  driving  of  Amoeba  (p.  185),  and  the  description  of  the 
method  by  which  Ama^ba  avoids  an  obstacle  (p.  186). 

Whether  these  actions  agree  with  the  accepted  idea  of  an  automatic 
action  in  being  unconscious  we  have,  of  course,  no  means  of  knowing. 

VARIABILITY    AND    MODIFIABILITY    OF   REACTIONS. 

JThere  is  little  that  can  be  said  on  this  point.  Verworn  (1890,  «,  p. 
271)  says  that  when  an  electric  current  is  passed  through  a  prepara- 
tion containing  many  Amoebae,  some  respond  strongly,  while  others 
do  not ;  thus  difterent  individuals  vary  in  their  responsiveness.  Fur- 
ther, a  given  individual  may  become  accustomed  to  the  current,  at  first 
responding  to  it,  later  not  responding.  Doubtless  such  phenomena  of 
acclimation  are  common  in  the  reactions  to  all  sorts  of  stimuli. 

Rhumbler  (1898,  p.  203)  shows  that  when  Amoebas  are  engaged  in 
taking  Oscillaria  filaments  as  food,  light  thrown  upon  them  modifies 
them  physiologically  in  such  a  way  that  they  eject  the  food.  The 
nature  of  the  reaction  is  thus  shown  to  depend  partly  on  the  physio- 
logical condition  of  the  animal. 

There  is  no  direct  experimental  evidence  as  yet,  so  far  as  I  am  aware, 
that  Amoeba  shows  memory.*  Experimental  evidence  as  to  whether 
the  reactions  of  a  given  Amoeba  to  a  given  stimulus  are  modified  by 
previous  stimuli  received  is  very  difficult  to  obtain,  principally  because 
it  is  practically  impossible  to  make  succeeding  stimuli  alike,  so  that 
one  cannot  tell  whether  a  difference  in  the  reaction  is  due  to  a  difier- 
ence  in  the  present  stimulus  or  not.  Possibly  there  is  a  faint  indication 
of  something  akin  to  memory  shown  in  the  facts  described  on  page  201. 
Here  a  smaller  Amoeba  which  had  been  ingested  as  prey  escaped  from 
the  posterior  end  of  the  captor  ;  the  latter  thereupon  reversed  its  move- 
ments, came  up  with  the  escaping  prey,  and  again  ingested  it.  In  the 
interval  between  the  complete  separation  of  the  prey  from  its  captor 
and  its  recapture,  the  behavior  of  the  captor  would  seem  to  have  been 
determined  by  some  trace  left  within  it  by  the  former  possession  of  the 

♦The  word  memorj  is,  of  course,  used  here  of  the  objective  phenomenon  that 
in  many  animals  present  behavior  is  modified  in  accordance  with  past  stimuli 
received,  or  past  reactions  given.  Of  possible  subjective  accompaniments  of  this 
objective  phenomenon  we,  of  course,  know  nothing  directlj  to  far  as  the  lower 
organisms  are  concerned. 


23©  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

prey.  But,  possibly,  this  trace  was  merely  of  a  gross  physical  char- 
acter, acting  as  a  direct  stimulus  to  produce  the  observed  behavior.  If 
this  is  true,  the  behavior  shows  no  indication  of  memory. 

SUMMARY. 

OBSERVATIONS. 
THE   USUAL    MOVEMENTS. 

(i)  Locomotion  in  Amoeba  is  a  process  that  may  be  compared  with 
rolling,  the  upper  and  lower  surfaces  continually  interchanging  posi- 
tions. This  is  shown  by  observation  of  the  movements  of  particles 
attached  to  the  outer  surface  or  embedded  in  the  ectosarc  of  the  animal. 
Such  attached  particles  move  forward  on  the  upper  surface  and  over 
the  anterior  edge,  remain  quiet  on  the  under  surface  till  the  body  of  the 
Amoeba  has  passed,  then  pass  upward  at  the  posterior  end  and  forward 
on  the  upper  surface  again.  Single  particles  may  thus  be  observed  to 
make  many  complete  revolutions.  (See  p.  170,  Fig.  58,  and  Figs.  38, 39, 
40,  41.)  * 

(2)  Thus  the  upper  surface  moves  forward  in  the  same  direction  as 
the  internal  currents,  while  the  lower  surface  is  at  rest.  There  is  char- 
acteristically no  backward  current  anywhere  in  Amoeba,  though  at 
times  some  of  the  endoplasmic  particles,  spreading  out  laterally  at  the 
anterior  end,  may  move  a  slight  distance  backward  at  the  sides.  This 
is  rare  (see  p.  134).  The  forward  current  on  the  upper  surface  is  not 
confined  to  a  thin  layer,  but  extends  inward  to  the  endosarc  ;  the  endo- 
sarcal  and  surface  currents  are  one  (p.  142). 

(3)  In  the  formation  of  pseudopodia  that  are  in  contact  with  the 
substratum  the  movement  of  protoplasm  is  identical  with  that  at  the 
anterior  end  of  the  Amoeba.  The  upper  surface  and  internal  contents 
flow  toward  the  tip,  while  the  surface  in  contact  with  the  substratum  is 
quiet.  Particles  adhering  to  the  upper  surface  are  carried  out  to  the  tip 
and  rolled  under  to  the  lower  surface,  where  they  remain  quiet  (p.  152). 

(4)  In  the  formation  of  pseudopodia  projecting  freely  into  the  water, 
the  movements  of  substance  are  the  same  as  in  pseudopodia  that  are  in 
contact,  save  that  there  is  no  part  of  the  surface  at  rest.     The  whole 

*  Of  anyone  who  is  inclined  to  reject  these  results  on  the  basis  of  previous 
observations,  or  of  their  supposed  incompatibility  with  other  known  facts,  let 
me  make  the  following  request:  Before  taking  ground  against  the  results,  pro- 
cure some  specimens  of  Amoeba  verrucosa  or  one  of  its  relatives.  This  is  usually 
easily  done.  Then  mix  thoroughly  with  the  water  containing  them  some  fine 
soot,  and  observe  carefully  the  movements  of  the  animals.  The  particles  attach 
themselves  to  the  outside,  and  the  movements  of  the  surface  are  then  observable 
with  the  greatest  ease.  It  is  such  a  simple  matter  to  determine  certain  of  the 
chief  points  for  one's  self  in  this  manner  that  it  would  be  regrettable  for  contro- 
versy to  arise  through  neglect  of  the  needed  observations. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  231 

surface  thus  moves  outward,  and  new  parts  of  the  surface  of  the  body 
continually  pass  on  to  the  pseudopodium.  An  object  adhering  to  the 
surface  of  the  pseudopodium  remains  at  approximately  the  same  dis- 
tance from  the  tip,  both  when  the  pseudopodium  is  short  and  when  it 
has  become  very  long  (pp.  153-156,  and  Figs.  47-49). 

(5)  In  the  withdrawal  of  a  free  pseudopodium  {a)  a  process  occurs 
that  is  the  reverse  of  that  described  in  (4),  the  surface  of  the  pseudo- 
podium passing  from  its  base  on  to  the  surface  of  the  body  (p.  156, 
and  Fig.  49) ;  (3)  the  surface  of  the  pseudopodium  becomes  wrinkled 
and  shrunken  ;   {c)  the  endosarc  flows  back  into  the  body. 

(6)  Any  part  of  the  protoplasm  may  be  excluded  temporarily  from 
the  forward  currents.  In  many  Amoebae  there  is  usually  a  region  at 
the  posterior  end  which  is  thus  temporarily  excluded  (the  posterior 
appendage,  tail).  In  such  cases  the  lower  surface  of  the  Amoeba 
passes  upward  on  each  side  of  this  appendage  to  become  part  of  the 
upper  surface,  then  passes  forward  (p.  169,  and  Fig.  57).  The  sub- 
stance of  the  posterior  appendage  is  itself  gradually  drawn  into  the 
forward  current. 

(7)  The  anterior  portion  of  the  advancing  Amoeba  is  attached  to  the 
substratum,  while  the  posterior  portion  isnot  (p.  165).  There  is  a  viscid 
secretion  produced  on  the  outer  surface  of  the  Amoeba,  to  which  the 
attachment  may  be  due. 

(8)  The  attached  anterior  portion  of  the  body  is  spread  out  and 
usually  very  thin.  The  unattached  posterior  portion  becomes  rounded 
and  thick,  and  is  contracting,  so  that  there  is  a  slight  forward  move- 
ment on  the  lower  surface,  as  well  as  on  the  upper  surface,  in  this  part 
(p.  166). 

(9)  All  the  activities  concerned  in  locomotion  can  be  performed  when 
the  animal  is  not  attached  to  the  substratum.  (But  for  progression  such 
attachment  is  necessary,  p.  215.) 

(10)  The  locomotion  of  Amoeba  is  similar  even  in  details  to  the 
movements  of  a  drop  of  inorganic  fluid  which  adheres  strongly  to  the 
substratum  at  one  edge  and  spreads  out  upon  it  here,  while  the  other 
edge  is  free  (pp.  209-214).  It  is  similar  in  most  respects  (except  in  the 
thinness  of  the  anterior  edge)  to  the  movements  under  the  influence  of 
gravity  of  a  drop  of  fluid  along  an  inclined  surface  to  which  it  adheres 
but  slightly. 

(11)  The  currents  in  a  moving  Amoeba  are  not  similar  to  those  of  a 
drop  of  inorganic  fluid  that  is  moving  or  elongating  as  a  result  of  a  local 
increase  or  decrease  in  surface  tension.  The  surface  currents  away 
from  the  region  of  least  tension  and  in  the  opposite  direction  to  the 
axial  currents  that  are  characteristic  of  such  a  drop  are  lacking  in 
Amoeba.  Here  surface  and  axial  currents  have  the  same  direction 
(p.  205). 


2^2  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

(12)  Similarly,  the  movements  of  material  in  a  forming  pseudo- 
podium  are  not  like  those  in  a  projection  which  is  produced  in  a  drop 
of  inorganic  fluid  as  a  result  of  a  local  decrease  in  surface  tension.  The 
surface  currents  away  from  the  tip  in  the  inorganic  projection  are  lack- 
ing in  Amoeba,  the  surface  here  moving  in  the  same  direction  as  the 
tip  (p.  206). 

(13)  The  body  of  Amoeba  shows  under  some  conditions  elasticity 
of  form,  such  as  is  characteristic  of  solids  (pp.  175-177)- 

(14)  Besides  the  movements  directly,  concerned  in  the  usual  loco- 
motion, limited  local  contractions  may  occur,  resulting  in  swinging  or 
vibratory  motions  of  the  pseudopodia  (p.  177),  or  in  sudden,  jerky 
movements  of  the  body  as  a  whole  (p.  179),  or  in  the  constricting  off 
of  parts  of  the  body  (p.  180). 

(15)  The  roughness  of  surface  in  a  retracting  pseudopodium,  the 
retention  of  irregular  forms  by  Amoeba,  and  the  movements  mentioned 
in  the  foregoing  paragraph,  are  similar  to  certain  phenomena  to  be 
observed  in  mixtures  of  solids  and  fluids,  as  a  result  of  the  interaction 
of  surface  tension  and  the  friction  of  the  solid  particles  (p.  215). 

REACTIONS    TO    STIMULI. 

(16)  The  following  reactions  are  described :  Positive  and  negative 
reactions  to  mechanical  stimuli  (pp.  1S1-187) ;  negative  reactions  to 
chemical  stimuli  (pp.  187-190);  negative  reaction  to  heat  (pp.  190-191); 
reaction  to  the  constant  electric  current  (pp.  191-192);  complex  reac- 
tions connected  with  food-taking  (pp.  193-202);  reactions  to  injuries 
(pp.  202-204). 

(17)  In  most  reactions  modifying  the  direction  of  motion  a  new 
advancing  wave  of  protoplasm  is  sent  out  from  some  part  of  that  por- 
tion of  the  body  which  is  already  attached  to  the  substratum.  The 
internal  and  surface  currents  then  flow  in  that  direction,  thus  changing 
the  course  of  the  animal.  Thus,  when  the  animal  changes  its  course  in 
a  reaction,  the  surface  currents  change  their  course  in  a  corresponding 
way,  as  shown  by  the  movements  of  particles  on  the  surface  (pp.  143, 
185,  192). 

(18)  Sometimes  the  course  is  squarely  reversed  as  a  result  of  a 
stimulus.  In  this  case  the  original  anterior  region  becomes  detached 
from  the  bottom,  while  a  new  pseudopodium  projects  freely  into  the 
water  from  the  former  posterior  (unattached)  region,  settles  down,  and 
becomes  attached ;  the  internal  and  surface  currents  then  follow  it. 
This  process  requires  usually  a  considerable  interval  of  time  (pp.  183, 

1S4). 

(19.)  Both  surface  currents  and  internal  currents  are  toward  the 
source  of  stimulation  in  a  positive  reaction,  away  from  the  source  of 
stimulation  in  a  negative  reaction. 


THE    MOVEMENTS    ANt>    REACTIONS    OF   AMCEBA.  2^'^ 

(20)  The  currents  in  the  positive  and  negative  reactions  are  not 
similar  to  the  currents  in  a  drop  of  inorganic  fluid  moving  toward  or 
away  from  an  agent  which  causes  a  local  decrease  or  increase  in  the 
surface  tension.  In  Amoeba  the  currents  on  the  surface  and  in  the 
interior  are  congruent :  in  the  inorganic  fluid  they  are  opposed. 

(21)  In  the  taking  of  food  the  protoplasm  and  the  food  body  in 
many  cases  do  not  tend  to  adhere,  so  that  the  Amoeba  is  compelled  to 
overcome  considerable  mechanical  difliculty  before  the  food  can  be 
inclosed.  Frequently  the  food  body  rolls  away  from  the  animal  as  soon 
as  it  is  touched  (pp.  193,  196).  The  difliculty  is  overcome  by  sending 
out  pseudopodia  on  each  side  of  the  body  and  inclosing  it,  together  with 
a  certain  amount  of  water.  In  Amoeba  verrucosa  and  its  relatives  food- 
taking  is  aided  by  the  tendency  of  foreign  bodies  to  adhere  to  the  body 
surface.  Amoebas  frequently  prey  upon  each  other,  and  this  often  gives 
rise  to  a  long  and  complex  train  of  reactions  (pp.  198-202,  and  Fig.  76). 

CONCLUSIONS. 

(22)  The  chief  factors  in  locomotion  seem  to  be  as  follows:  (i)  At 
the  anterior  edge  of  the  Amoeba  a  wave  of  protoplasm  pushes  out,  rolls 
over,  and  becomes  attached  to  the  substratum  ;  (2)  This  pulls  on  the 
upper  surface  of  the  Amoeba,  causing  it  to  move  forward  ;  (3)  The 
hinder  portion  of  the  Amoeba  becomes  released  from  the  substratum, 
and  contracts  slowly  ;  (4)  As  a  result  of  the  strong  pull  from  in  front 
and  the  slight  contraction  from  behind  the  posterior  end  moves  forward  ; 
(5)  The  internal  substance  must  flow  forward  as  a  result  of  the  pull  on 
the  upper  surface,  the  movement  forward  of  the  posterior  end,  and  the 
pressure  due  to  the  pulling  from  in  front  and  the  contraction  behind. 
The  movement  of  the  internal  fluid  is  comparable  to  that  in  a  sac  or 
bladder  half  filled  with  water  and  rolled  along  a  surface  (pp.  146,  149, 

.7.). 

(23)  There  is  no  continuous  transformation  of  endosarc  into  ectosarc 
at  the  anterior  end,  and  of  ectosarc  into  endosarc  behind  this  (Rhum- 
bler's  ento-ectoplasm  process),  as  a  necessary  feature  of  locomotion, 
since  the  ectosarc  of  the  upper  surface  rolls  over  to  the  under  surface 
at  the  anterior  end  (p.  14S).  Nevertheless,  ectosarc  and  endosarc  are 
mutually  interconvertible  when  need  arises  for  the  change  of  one  into 
the  other. 

(24)  It  results  from  paragraphs  (i),  (2),  (11),  above,  that  the  loco- 
motion of  Amoeba  cannot,  with  fidelity  to  the  results  of  the  physical 
experiments,  be  accounted  for  by  a  decrease  in  surface  tension  at  the 
anterior  end. 

(25)  From  (3),  (4),  (12),  above,  we  must  conclude  that  the  sending 
out  of  pseudopodia  cannot,  without  violence  to  the  results  of  the  phys- 
ical experiments,  be  accounted  for  as  due  to  a  local  decrease  in  surface 
tension  at  the  point  of  the  pseudopodium. 


334  "^^^   BEHAVIOR   OF   LOWER    ORGANISMS. 

(26)  From  (i)  and  (10)  above  it  results  that  the  simple  locomotion 
on  a  substratum  could,  taken  by  itself,  be  accounted  for  on  Berthold's 
theory  that  the  movement  is  due  to  the  spreading  out  of  a  fluid  on  a 
solid.  But  this  theory  fails  when  we  take  into  account  the  formation 
of  free  pseudopodia  (p.  214),  and  the  fact  that  all  the  processes  con- 
cerned in  locomotion  can  be  performed  without  adherence  to  a  solid 
(paragraph  (9)  above). 

(27)  From  (3),  (4),  (9),  (11),  (12),  (34),  (25),  (26),  we  must  con- 
elude  that  the  formation  of  pseudopodia  and  the  sending  out  of  waves 
of  protoplasm  at  the  anterior  end  of  a  moving  Amoeba  are  due  to  a 
local  activity  of  the  protoplasm  for  which  no  physical  explanation  has 
been  given.  Since  these  are  the  essential  features  in  locomotion,  we 
must  conclude  that  locomotion  in  Amoeba  has  not  been  physically 
explained. 

(28)  From  (17),  (19),  (20),  it  follows  that  we  cannot,  with  fidelity 
to  the  results  of  physical  experimentation,  hold  that  the  effects  of  stimuli 
in  modifying  the  movements  of  Amoeba  are  due  to  their  direct  (or  even 
indirect)  action  in  changing  the  surface  tension  of  the  parts  affected. 

(29)  From  (21)  we  must  conclude  that  adherence  between  the  proto- 
plasm and  the  food  substance  does  not  furnish  an  adequate  explanation 
of  food-taking  and  the  choice  of  food  in  Amoeba. 

(30)  From  (24),  (25),  (27),  (28),  we  must  conclude  that  changes  in 
the  surface  tension  of  the  body  are  not  the  primary  factors  in  the  move- 
ments and  reactions  of  Amoeba.     (See  note,  p.  225). 

(31)  All  the  results  taken  together  lead  to  the  conclusion  that  neither 
the  usual  movements  nor  the  reactions  of  Amoeba  have  as  yet  been 
resolved  into  known  physical  factors.  There  is  the  same  unbridged 
gap  between  the  physical  effect  of  the  stimulus  and  the  reaction  of  the 
organism  that  we  find  in  higher  animals. 

(32)  In  the  behavior  of  Amoeba  we  may  distinguish  factors  compar- 
able to  the  habits,  reflexes,  and  automatic  activities  (Ziehen)  of  higher 
organisms  (pp.  228-229).  Its  reactions  as  a  rule  are  adaptive  (pp. 
227-228). 


SEVENTH    PAPER 


THE  METHOD  OF  TRIAL  AND  ERROR  IN  THE 
BEHAVIOR  OF  LOWER  ORGANISMS. 


235 


THE  METHOD  OF  TRIAL  AND  ERROR  IN  THE 
BEHAVIOR  OF  LOWER  ORGANISMS. 


A  certain  type  of  behavior  in  higher  animals  has  been  characterized 
by  Lloyd  Morgan  as  the  method  of  trial  and  error.  The  nature  of  such 
behavior  is  well  brought  to  mind  by  an  example  from  Morgan  (1894, 
p.  257).  His  dog  was  required  to  bring  a  hooked  walking  stick 
through  a  narrow  gap  in  a  fence.  The  dog  did  not  pause  to  consider 
that  the  stick  would  pass  through  the  narrow  opening  only  if  taken 
by  one  end  and  pulled  lengthwise.  On  the  contrary,  he  simply  seized 
the  stick  in  the  way  that  happened  to  be  most  convenient,  near  its 
middle,  and  tried  to  carry  it  through  the  gap  in  the  fence  in  that  man- 
ner. Of  course,  the  stick  would  not  pass,  and  after  some  effort  the 
dog  was  forced  to  drop  it.  Then  he  seized  it  again  at  random,  and 
made  a  new  effort.  Again  the  stick  was  stopped  by  the  fence  ;  again 
the  dog  dropped  it,  took  a  new  hold,  and  tried  again.  After  several 
repetitions  of  this  performance,  the  dog  seized  the  stick  by  the  hooked 
end.     This  time  it  passed  through  the  gap  in  the  fence  easily. 

The  dog  had  "tried"  all  possible  methods  of  pulling  the  stick 
through  the  fence.  Most  of  the  attempts  showed  themselves  to  be 
*'  error.'*  Then  the  dog  tried  again,  till  he  finally  succeeded.  Thus 
he  worked  by  the  method  of  trial  and  error. 

This  method  of  reaction  has  been  found  by  Lloyd  Morgan,  Thorn- 
dike  (1S9S),  and  others,  to  play  a  large  part  in  the  development  of 
intellieence  in  hijjher  animals.  Intelligfent  action  arises  as  follows: 
The  animal  works  by  the  method  of  trial  and  error  till  it  has  come 
upon  the  proper  method  of  performing  an  action.  Thereafter  it  begins 
with  the  proper  way,  not  performing  the  trials  anew  each  time.  Thus 
intelligent  action  has  its  basis  in  the  method  of  "  trial  and  error,"  but 
does  not  abide  indefinitely  in  that  method. 

Behavior  having  the  essential  features  of  the  method  of  "  trial  and 
error"  is  widespread  among  the  lower  and  lowest  organisms,  though 
it  does  not  pass  in  them  so  immediately  to  intelligent  action.  But  like 
the  dog  bringing  the  stick  through  the  fence  the  first  time,  they  try  all 
ways,  till  one  shows  itself  practicable. 

This  is  the  general  plan  of  behavior  among  the  lowest  organisms 
under  the  action  of  the  stimuli  which  pour  upon  them  from  the  sur- 
roundings. On  receiving  a  stimulus  that  induces  a  motor  reaction, 
they  try  going  ahead  in  various  directions.  When  the  direction  fol- 
lowed leads  to  a  new  stimulus,  they  try  another,  till  one  is  found  which 
does  not  lead  to  efi'ective  stimulation. 

237 


238 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


>»^: 


This  method  of  trial  and  error  is  especially  well  developed  in  free- 
swimming  single-cell  organisms — the  flagellate  and  ciliate  infusoria — 
and  in  higher  animals  living  unde  similar  conditions,  as  in  the  Roti- 
fera.  In  these  creatures  the  structure  and  the 
method  of  locomotion  and  reaction  are  such 
as  to  seem  cunningly  devised  for  permitting 
behavior  on  the  plan  of  trial  and  error  in  the 
simplest  and  yet  most  effective  way. 

These  organisms,  as  they  swim  through  the 
water,  typically  revolve  on  the  long  axis,  and  at 
the  same  time  swerve  toward  one  side,  which 
is  structurally  marked.  This  side  we  will  call 
X.  Thus  the  path  becomes  a  spiral.  The  or- 
ganism is,  therefore,  even  in  its  usual  course, 
successively  directed  toward  many  different 
points  in  space.  It  has  opportunity  to  try  suc- 
cessively many  directions  though  still  progress- 
ing along  a  definite  line  which  forms  the  axis 
of  the  spiral  (see  Fig.  79).  At  the  same  time 
the  motion  of  the  cilia  by  which  it  swims  is 
pulling  toward  the  head  or  mouth  a  little  of  the 
water  from  a  slight  distance  in  advance  (Fig. 
79).  The  organism  is,  as  it  were,  continually 
taking  "samples"  of  the  water  in  front  of  it. 
This  is  easily  seen  when  a  cloud  of  India  ink 
is  added  to  the  water  containing  many  such 
organisms. 

At  times  the  sample  of  water  thus  obtained  is 
of  such  a  nature  as  to  act  as  a  stimulus  for  a 
motor  reaction.  It  is  hotter  or  colder  than 
usual,  or  contains  some  strong  chemical  in  solu- 
tion, perhaps.  Thereupon  the  organism  reacts 
in  a  very  definite  way.  At  first  it  usually 
stops  or  swims  backward  a  short  distance,  then 
it  swings  its  anterior  end  farther  than  usual 
toward  the  same  side  X  to  which  it  is  al- 
ready swerving.  Thus  its  path  is  changed. 
After  this  it  begins  to  swim  forward  again.  The  amount  of  backing 
and  of  swerving  toward  the  side  X  is  greater  when  the  stimulus  i^  more 
intense. 


Fig. 


79- 


*FiG.  79. — Spiral  path  in  the  ordinary  swimming  of  Paramecium,  showing 
how  the  anterior  end  is  pointed  successively  in  different  directions,  and  how  a 
sample  of  water  is  drawn  to  the  anterior  end  and  mouth  from  each  of  these 
directions. 


Volume  XI,  Part  2 

CONTRIBUTIONS 


TO  THE 


STUDY  OF  THE  BEHAVIOR 
OF  LOWER  ORGANISMS 


BY 


HERBERT  S.  JENNINGS 

Assistant  Professor  of  Zoology,  University  of  Pennsylvania 
Research  Assistant,  Carnegie  Institution  of  Washington 


Published  by  the  Carnegie  Institution 

OF  Washington 

1904 


CONTRIBUTIONS 


TO  THE 


STUDY  OF  THE  BEHAVIOR 
OF  LOWER  ORGANISMS 


BY 


HERBERT  S.  JENNINGS 

Assistant  Professor  of  Zoology,  University  of  Pennsylvania 
Research  Assistant,  Carnegie  Institution  of  Washington 


Published  by  the  Carnegie  Institution 

OF  Washington 

1904 


Carnegie  Institution  of  Washington, 
Publication  No.   i6. 


Press  of  Gibson  Bros. 
Washington,  D.  C. 


PREFATORY  NOTE. 


The  investigations  the  results  of  which  are  herein  set  forth  were 
carried  out  by  the  aid  of  certain  grants  from  the  Carnegie  Institution 
of  Washington.  The  author  desires  to  express  his  deep  sense  of  obli- 
gation for  the  aid  thus  rendered.  The  first  five  papers  were  prepared 
at  the  Zoological  Laboratory  of  the  University  of  Michigan,  and  were 
submitted  to  the  Carnegie  Institution  for  publication  August  i,  1903. 
To  the  third  paper  some  additions  were  made  in  February,  1904. 
The  sixth  and  seventh  papers  were  prepared  at  the  Naples  Zoological 
Station,  while  the  writer  was  acting  as  Research  Assistant  of  the 
Carnegie  Institution,  and  were  transmitted  for  publication  in  January 
and  March,  respectively,  1904. 


LIST  OF  PAPERS. 


1.  Reactions  to  Heat  and  Cold  in  the  Ciliate  Infusoria. 

2.  Reactions  to  Light  in  Ciliates  and  Flagellates. 

3.  Reactions  to  Stimuli  in  Certain  Rotifera. 

4.  The  Theory  of  Tropisms. 

5.  Physiological    States   as    Determining   Factors    in   the  Behavior   of   Lower 

Organisms. 

6.  The  Movements  and  Reactions  of  Amoeba. 

7.  The  Method  of  Trial  and  Error  in  the  Behavior  of  Lower  Organisms. 


FIRST    PAPER. 


REACTIONS  TO  HEAT  AND  COLD 
IN  THE  CILIATE  INFUSORIA. 


REACTIONS  TO  HEAT  AND  COLD  IN  THE 
CILIATE   INFUSORIA. 


To  explain  the  movements  of  organisms  toward  or  from  a  source  of 
stimulus,  we  find  given  almost  universally  in  one  shape  or  another  a 
certain  general  formula.  This  is  the  schema  set  forth,  with  unessen- 
tial variations,  by  Verworn  (1899,  pp.  500-502)  for  the  orientation  of 
a  ciliate  or  flagellate  infusorian  to  a  one-sided  stimulus,  and  by  Loeb 
(1S97,  PP'  439~442)  for  the  tropisms  of  organisms  in  general.  Essen- 
tially, the  schema  is  as  follows  :  An  agent  acting  upon  the  organism 
from  one  side  causes  the  locomotor  organs  of  that  side  to  contract 
either  more  strongly  or  less  strongly  than  those  of  the  opposite  side. 


Fig.  I.* 

In  the  former  case  (Fig.  i)  the  animal  is  turned  away  from  the  source 
of  stimulus,  till  it  comes  into  a  position  in  which  the  motor  organs  of 
the  two  sides  are  similarly  affected.  Then  progressing  straight  for- 
ward, it  of  course  moves  away  from  the  source  of  stimulus  (negative 
taxis  or  tropism).  If  the  motor  organs  on  the  side  most  affected  are 
caused  to  contract  less  strongly  than  those  on  the  opposite  side  (Fig.  2) 


*FiG.  1. — Diagram  of  a  negative  reaction  of  an  organism,  according  to  the 
tropism  schema.  The  motor  organs  which  act  more  effectively  are  shown  more 
heavily  drawn.  The  more  pointed  end  is  the  anterior.  A  stimulus  is  supposed 
to  impinge  upon  the  organism  a  from  the  direction  indicated  by  arrows;  this 
causes  the  motor  organs  directly  affected  by  the  stimulus  to  beat  more  strongly, 
as  indicated  by  the  darker  shade.  The  result  is  to  turn  the  anterior  end  in  the 
direction  indicated  by  curved  arrows.  The  organism  thus  occupies  successively 
the  positions  «,  b,  c,  finally  coming  into  the  position  d.  Here  the  motor  organs 
of  the  two  sides  are  equally  affected  by  the  stimulus,  hence  there  is  no  further 
cause  for  a  change  of  position.  The  usual  forward  motion  of  the  organism  now 
takes  it  away  from  the  source  of  stimulus,  as  indicated  by  the  straight  arrow  at  d. 

7 


THK  BEHAVIOR  OF  LOWER  ORGANISMS. 


the  organism  is  necessarily  turned  witii  anterior  end  toward  the  source 
of  stimulus ;  then  its  usual  forward  movements  take  it  toward  the 
source  of  stimulus  (positive  taxis  or  tropism).  Loeb  lays  especial 
stress  on  the  direction  from  which  the  stimulus  comes,  as  it  is  this 
that  determines  which  side  shall  be  most  strongly  affected  by  the 
stimulus  ;  otherwise  the  theory  as  he  sets  it  forth  is  essentially  like  that 
held  by  Verworn.  Both  these  authors  apply  this  schema  to  the  move- 
ments of  organisms  to  and  from  many  sorts  of  stimuli,  making  it  a 
general  formula  for  taxis  or  iropisms.     Verworn  says  (1899,  p.  503): 

Thus  the  phenomena  of  positive  and  negative  chemotaxis,  thermotaxis,  photo- 
taxis  and  galvanotaxis,  which  are  so  highly  interesting  and  important  in  all  or- 
ganic life,  follow  with  mechanical  necessity  as  the  simple  results  of  differences 
in  biotonus,  which  are  produced  by  the  action  of  stimuli  at  two  different  poles  of 
the  free  living  cell. 

In  the  present  series  of  papers  the  writer  proposes  to  examine  the 
behavior  of  a  number  of  lower   organisms,   in   order  to   determine 


Fig.  2.* 

whether  the  reactions  to  the  usual  stimuli  take  place  in  accordance 
with  this  tropism  schema  or  not,  and  if  not,  to  determine  the  real 
nature  of  the  reaction  method.  In  this  first  paper  we  shall  deal  with 
reactions  to  heat  and  cold. 

In  his  recent  series  of  papers  on  the  reactions  of  infusoria  to  heat  and 
cold,  Mendelssohn  (1902,  «,  <5,  c)  develops  a  theory  of  thermotaxis  in 
accordance  with  the  general  theory  of  tropisms,  above  set  forth.  In  an 
earlier  paper  (Jennings,  1899)  ^^^  present  author,  on  the  other  hand. 


♦Fig.  2. — Diagram  of  a  positive  reaction,  according  to  the  tropism  schema. 
A  stimulus  coming  from  the  direction  indicated  by  the  arrows  to  the  right  acts 
upon  the  organism  a.  The  effect  of  the  stimulus  is  to  cause  the  motor  organs 
directly  affected  by  it  to  contract  less  strongly,  as  indicated  by  the  lighter  shade 
on  the  right  side  of  a.  As  a  result  the  animal  is  turned  as  shown  by  the  curved 
arrows,  occupying  successively  the  positions  a,  by  c,  d.  At  d  the  stimulus 
affects  the  two  sides  alike,  hence  there  is  no  cause  for  further  turning,  and  the 
usual  forward  movement  of  the  organism  takes  it  toward  the  source  of  stimulus. 


REACTIONS  TO  HEAT  AND  COLD. 


gave  a  brief  account  of  the  reactions  of  Paramecium  to  heat  and  cold, 
according  to  which  these  reactions  are  quite  inconsistent  with  the 
tropism  schema.  As  the  matter  is  one  of  considerable  interest,  and  the 
conclusions  reached  by  Mendelssohn  and  myself  seem  quite  irrecon- 
cilable, I  have  examined  anew  the  phenomena  in  a  considerable  number 
of  infusoria,  including  Paramecium. 

The  general  phenomena  to  be  explained  are  well  seen  in  the  follow- 
ing experiment,  taken  from  Mendelssohn  (Fig.  3).  An  ebonite  trough 
10  cm.  in  length  and  2  cm.  wide  is  filled  with  water  containing  Para- 
mecia  (a).  Now,  by  proper  methods,  one  end  of  the  trough  is  slowly 
heated  to  38°,  while  the  other  is  kept  at  the  temperature  26°.     The 


a 

T — : 5—7*": — y  -  "<  ■-— ■» — r-= 

IS' 

13 

i 

26'-                 - — 

38 

c 

L 

10 


25' 


Fig.  3.* 

Paramecia  soon  leave  the  heated  region,  traveling  away  from  it  in  a 
rather  compact  mass,  and  in  5  to  15  minutes  they  have  reached  the  op- 
posite end  (3) .  If  now  the  temperature  at  the  two  ends  is  reversed, 
the  Paramecia  travel  back  to  the  end  from  which  they  came.  If  the 
temperature  is  lowered  to  10°  at  one  end,  instead  of  raised,  similar  re- 
sults are  obtained ;  the  Paramecia  leave  the  cold  region,  as  before  they 


*  Fig.  3. — General  phenomena  of  thermotaxis  in  Paramecium,  after  Men- 
delssohn (1902,  a).  At  a  the  Paramecia  are  placed  in  an  ebonite  trough,  both 
ends  of  which  have  a  temperature  of  19°.  The  Paramecia  are  equallj  scattered. 
At  3,  the  temperature  of  one  end  is  raised  to  38°,  while  at  the  other  it  is  only  26°. 
The  Paramecia  collect  at  the  end  having  the  lower  temperature  ("negative 
thermotaxis").  At  c,  one  end  has  a  temperature  of  25°,  while  the  other  is 
lowered  to  10°.  The  Paramecia  now  gather  at  the  end  having  the  higher  tem- 
perature ("positive  thermotaxis"). 


lO  THE    BEHAVIOR    OF    I.OWKR    ORGANISMS. 

left  the  heated  region  (c).  If  one  end  is  heated,  while  the  other  is 
cooled,  the  Paramecia  gather  in  the  intermediate  region. 

How  are  these  movements  to  be  explained?  Mendelssohn  applies 
to  the  phenomena  Verworn's  schema  for  the  orientation  of  a  ciliate 
organism  to  a  one-sided  stimulus  (see  Figs,  i  and  2).  As  we  wish  to 
deal  thoroughly  with  this  schema,  it  will  be  well  to  set  it  forth  here,  as 
applied  by  Mendelssohn  to  heat  and  cold,  with  some  fullness. 

The  temperature  being  higher  at  one  end  of  the  trough  than  at  the 
other,  that  side  or  end  of  the  animal  directed  to  the  heated  end  of  the 
trough  has  a  higher  temperature  than  has  the  opposite  side  or  end 
(see  Fig.  4).  This  difference  in  temperature  causes  a  difference  in  the 
beat  of  the  cilia.  In  negative  thermotaxis  the  higher  temperature 
causes  the  cilia  to  contract  more  strongly,  as  indicated  by  the  heavier 
shade  (on  the  left  side)  in  the  figure ;  hence  the  animal  is  turned 
toward  the  opposite  side,  or  away  from  the  source  of  heat,  until  it 
comes  into  a  position  where  the  heat  acts  equally  on  the  two  sides. 
The  Paramecium  then  of  course  has  its  anterior  end  directed  from  the 

heated  region,  and  its  ordinary 


swimming  carries  it  away.  In 
positive  thermotaxis,  on  the 
other  hand,  the  lower  tempera- 
ture causes  stronger  contrac- 
FiG.A*  tions ;  hence  the  cilia  on   the 

side  np xt  the  cold  region  con- 
tract more  strongly,  turning  the  anterior  end  in  the  opposite  direction. 
The  Paramecium  then  swims  away,  as  a  result  of  its  normal  forward 
movement. 

Mendelssohn  studied  the  subject  primarily  from  a  quantitative  stand- 
point, determining  the  optimum  temperature,  the  rate  of  reaction,  the 
effects  of  different  temperatures,  etc.  For  this  purpose  he  constructed 
a  very  ingenious  and  delicate  apparatus,  which  permitted  accurate 
quantitative  results.  Relying  then  upon  his  valuable  papers  for  these 
matters,  I  have  devoted  myself  entirely  to  a  study  of  the  mechanism  of 
the  reactions.     For  this  purpose  an  apparatus  was  used  that  is  similar 


♦  Fig.  4. — Diagram  of  the  thermotactic  reaction  of  Paramecium  as  conceived 
by  Mendelssohn,  after  Mendelssohn  (1902,  d).  The  heavier  cilia  on  the  left  side 
show  those  contracting  most  strongly  and  hence  those  most  effective  in  turning 
the  organism  or  driving  it  forward.  In  negative  thermotaxis  the  left  end  would 
have  the  higher  temperature,  causing  the  cilia  of  the  left  side  of  the  organism 
a  to  beat  more  strongly.  As  a  result,  the  organism  turns,  occupying  suc- 
cessively the  positions  a,  if,  c,  d.  In  the  latter  position  there  is  no  further 
cause  for  turning,  and  the  animal  swims  directly  away  from  the  heated  end. 
The  same  diagram  illustrates  also  positive  thermotaxis,  if  the  left  end  is  sup- 
posed to  be  cooled  below  the  optimum. 


REACTIONS    TO    lEEAT    AND    COLD. 


II 


in  principle  to  that  of  Mendelssohn,  but  more  easily  constructed  and 
permitting  exact  observation  of  the  organisms  with  the  microscope, 
though  otherwise  much  less  elegant  than  Mendelssohn's.  This  ap- 
paratus is  shown  in  Fig.  5.  It  consists  essentially  of  three  glass  tubes, 
of  8  millimeters  bore,  which  are  supported  in  a  horizontal  position, 
side  by  side,  by  passing  them  through  auger  holes  in  a  block  of 
wood.  The  tubes  are  one  inch  apart  and  are  placed  exactly  at 
the  same  level,  so  that  a  glass  slide  rests  equally  on  all  three.  To 
the  two  ends  of  each  of  these  rubber  tubes  are  attached.  The  rubber 
tubes  from  one  end  pass  upward  into  vessels  of  water  raised  on  a  shelf 
above  the  level  of  the  apparatus.     From  the  other  end  the  rubber  tubes 


pass  downward  into  a  waste  pail,  thus  acting  as  overflow  tubes.  A 
trough,  or  slide  (5),  containing  infusoria,  is  placed  on  the  three  glass 
tubes ;  the  water  in  the  vessels  on  the  shelf  is  heated  or  cooled  to  any 
desired  temperature,  and  is  then  siphoned  off  and  allowed  to  flow 
downward  through  the  glass  tubes.  The  rate  of  flow  is  controlled  by 
pinchcocks.  In  this  manner  heated  water  can  be  caused  to  flow 
beneath  one  end  of  the  slide,  cold  water  beneath  the  other.  The  slide 
being  thus  unequally  warmed,  the  reactions  of  the  organisms  can  be 
observed.  The  rubber  tubes  leading  from  the  hot  and  cold  vessels  can 
be  interchanged,  so  that  the  temperature  at  either  end  or  the  middle  of 
the  slide  can  be  at  once  changed  and  made  high  or  low,  without  the 

♦Fig.  5. — Apparatus   used   for   testing   reaction  to  heat  and  cold.      For  de- 
scription, see  text. 


12  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

slightest  disturbance  to  the  slide  or  trough  containing  the  organisms. 
The  plan  of  this  apparatus  is  taken  from  that  of  Mendelssohn.  It  can 
be  readily  constructed  in  an  hour  or  less,  and  gives  essentially  the  same 
results  as  Mendelssohn's  more  elaborate  arrangement.  With  the  use 
of  specially  constructed  thermometers,  such  as  were  employed  by 
Mendelssohn,  exactly  the  same  quantitative  work  could  be  done.  The 
present  apparatus  has  the  advantage  that  it  is  possible  to  place  a 
mirror  beneath  the  glass  slide  or  trough  bearing  the  organisms,  and 
thus  to  observe  the  movements  of  the  latter  with  the  microscope  by  the 
aid  of  reflected  light.  With  the  long-armed  Braus-Driiner  stand  the 
whole  extent  of  the  trough  can  be  examined  at  ease,  and  the  movements 
of  the  organisms  accurately  observed  with  the  stereoscopic  binocular. 

As  a  trough  I  usually  employed  a  glass  slide,  to  which  strips  of  glass 
2  mm.  in  diameter  had  been  cemented,  making  a  trough  3  inches  long, 
about  two-thirds  of  an  inch  wide,  and  2  mm.  deep.  In  some  of  the 
experiments  the  trough  was  covered  with  a  glass  plate ;  in  others  it 
was  left  open.     Both  methods  have  their  advantages  and  disadvantages. 

To  realize  the  exact  conditions  under  which  the  organisms  are  act- 
ing it  is  necessary  to  consider  a  further  question  :  What  is  the  precise 
nature  of  the  stimulating  agent  in  these  experiments.'*  Are  we  dealing 
with  radiant  heat  or  with  conducted  heat.f*  If  we  are  dealing 
primarily  with  radiant  heat,  of  course  currents  in  the  water  have 
no  effect  on  the  distribution  of  the  stimulating  agent.  If,  on  the  other 
hand,  we  are  dealing  with  conducted  heat,  if  the  stimulating  agent  is 
the  heated  or  cooled  water,  then  the  conditions  are  different.  Local 
currents  will  cause  local  variations  in  the  distribution  of  the  heated 
water.  It  is  evident,  I  think,  that  the  second  alternative  is  in  all 
probability  the  correct  one.  Certainly  in  a  bath-tub  or  in  a  long 
vessel  of  any  sort  in  which  the  water  is  heated  at  one  end  and  not  at 
the  other,  it  is  possible  by  producing  currents  to  vary  the  distribution 
of  the  heated  water  and  to  perceive  with  the  hand  that  it  is  this  heated 
water  which  acts  as  the  stimulus. 

The  importance  of  these  considerations  is  evident  when  we  take  into 
account  the  fact  that  the  ciliate  infusoria  are  always  accompanied  by 
currents  of  typical  character,  having  a  definite  relation  to  the  form  and 
orientation  of  the  animal's  body.  As  a  result  of  these  currents,  the  in- 
fusorian  becomes  not  a  mere  passive  recipient  of  stimulations,  but  an 
active  agent,  determining  by  its  activity  how  and  in  what  part  of  the 
body  it  shall  be  affected  by  stimuli.  This  may  be  illustrated  by  a 
diagram  (Fig.  6)  showing  the  typical  currents  produced  by  the  cilia 
of  Paramecium  and  the  effect  produced  by  these  currents  upon  the 
distribution  of  the  heated  (or  cooled)  water.     The  temperature  is  con- 


REACTIONS    TO    HEAT    AND    COLD. 


13 


ceived  to  be  greatest  to  the  right  of  the  figure  and  to  fall  off  regu- 
larly toward  the  left,  the  lines  indicating  regions  of  equal  temperature. 
The  last  line  to  the  left  is  marked  28°,  this  being  about  the  threshold 
temperature  for  the  negative  reaction  of  Paramecium,  according  to 
Mendelssohn.  The  space  about  the  Paramecium  (without  lines)  is  at 
a  temperature  below  28° — say  at  the  room  temperature — so  that  it 
does  not  act  as  a  stimulus  to  cause  movement.      Now,  as  the  diagram 


Fig.  6.* 

shows,  a  cone  of  water  is  drawn  toward  the  anterior  end  of  Para- 
mecium, from  a  considerable  distance  away,  necessarily  therefore 
including  water  above  the  threshold  temperature  of  28°.    This  cone  or 

♦Fig.  6. — Diagram  of  currents  produced  by  the  cilia  in  Paramecium  when 
the  animal  is  nearly  or  quite  at  rest.  At  right  of  the  line  marked  28°  the  tem- 
perature is  above  the  optimum  (above  28°)  while  at  the  left  of  this  line  it  is  at 
the  normal  or  optimum  temperature.  The  heated  water  first  reaches  the  Para- 
mecium at  the  anterior  end  on  the  oral  side,  passing  down  the  oral  groove  to 
the  mouth. 


14  THE    BEHAVIOR    OF   I.OWER    ORGANISMS. 

vortex  of  water  passes  as  a  slender  stream  along  the  oral  groove  of 
Paramecium  to  the  mouth.  Consequently,  water  heated  above  the 
threshold  temperature  reaches  the  Paramecium  in  this  region  before  it 
touches  the  body  elsewhere.  The  result  is  thus  a  stimulation  on  the 
oral  side  of  the  body,  not  elsewhere. 

Thus  the  way  in  which  the  organism  is  stimulated  depends  not  ex- 
clusively on  the  physical  laws  of  the  distribution  of  heat,  but  upon  the 
activity  of  the  organism  ;  and  the  method  of  reaction,  as  we  shall  see, 
is  of  a  corresponding  character. 

It  is  not  difficult  to  observe  the  distribution  of  the  currents  above 
described  if  one  adds  to  the  water  on  one  side  of  the  nearly  or  quite 
quiet  infusorian  a  cloud  of  very  finely  ground  India  ink.  The  same 
results  are  obtained  with  other  infusoria ;  in  Stentor,  in  Bursaria,  and 
in  some  of  the  larger  Hypotricha  the  results  are  particularly  striking. 
Of  course  if  the  India  ink,  or  the  surface  of  threshold  temperature,  is 
advancing  obliquely  to  the  axis  of  the  infusoria,  the  results  are  more 
complicated,  and  a  diagram  such  as  we  have  in  Fig.  6  is  not  easy  to 
construct.  But  the  result  is  uniformly  to  bring  the  stimulating  agent 
to  the  peristome  before  it  reaches  any  other  part  of  the  body.  It  is  not 
possible  to  observe  directly  the  distribution  of  water  of  different  tem- 
peratures, but  under  the  influence  of  currents  this  of  course  follows, 
essentially,  the  same  laws  as  do  fine  particles  suspended  in  the  water. 

Another  factor  which  it  is  important  to  take  into  consideration  in 
studying  the  effects  of  heat  or  other  agents  on  the  infusoria  is  the 
greater  sensitiveness  of  the  anterior  end  and  oral  surface  (or  peristome) 
as  compared  with  the  remainder  of  the  body.  This  the  present  writer 
has  demonstrated  for  the  anterior  end  by  direct  mechanical  stimulation 
in  a  considerable  number  of  infusoria  (Jennings,  1900),  while  Roesle 
(1902)  has  shown  a  similar  high  comparative  sensitivity  for  the  peri- 
stome region.  The  difference  is  such  that  in  many  cases  where  the 
animal  is  completely  enveloped  by  a  stimulating  agent  (as  by  a  chemi- 
cal, or  by  warm  or  cold  water)  there  is  reason  to  think  that  the 
reaction  given  is  due  to  the  stimulation  at  these  regions  alone.  In 
other  words,  the  stimulus  reaches  its  threshold  value  for  the  anterior 
end  and  the  region  about  the  mouth  much  before  it  reaches  this  value 
for  the  rest  of  the  body.  This  consideration  has  an  important  bearing 
on  the  theory  which  is  frequently  maintained,  that  the  directive  action 
of  a  stimulus  is  due  to  the  difference  in  its  intensity  on  the  two  ends  or 
sides  of  the  organism.  Even  if  a  stimulating  agent  acts,  per  se, 
slightly  more  strongly  on  the  posterior  end  than  on  the  anterior  end 
of  an  infusorian,  there  is  reason  to  think  that  the  reaction  would  be 
conditioned  entirely  by  the  stimulus  at  the  anterior  end,  this  reaching 


REACTIONS    TO    HEAT    AND    COLD.  I5 

its  threshold  value  before  the  stimulus  elsewhere  produces  any  effect. 
Corresponding  statements  could  be  made  with  relation  to  the  oral  and 
aboral  sides.  Of  course,  owing  to  the  course  of  the  currents  above 
described,  any  stimulating  agent  whose  distribution  is  affected  by  cur- 
rents in  the  water  will  usually  reach  the  anterior  end  and  oral  side 
first  in  any  case. 

Summing  up,  we  find  (i)  that  the  threshold  intensity  of  a  stimulating 
agent  whose  distribution  is  affected  by  currents  in  the  water  will  reach 
the  anterior  end  and  oral  side  of  the  organism  before  it  reaches  other 
parts  of  the  body ;  (2)  that  the  anterior  end  and  oral  surface  are  more 
sensitive  than  the  rest  of  the  body,  so  that  the  threshold  value  for 
stimuli  is  less  here  than  elsewhere. 

We  may  now  proceed  to  an  account  of  the  observed  method  by 
which  some  of  the  organisms  react  to  heat  and  cold. 

Oxytricha  fallax :  This  is  one  of  the  most  favorable  of  the  Ciliata 
for  determining  the  method  of  reactions  to  stimuli,  for  two  reasons, 
(i)  It  is  easil}'  procurable  in  large  numbers,  occurring  in  cultures  of 
the  same  sort  that  produce  Paramecium,  and  in  equal  abundance. 
(2)  It  does  not,  as  a  rule,  revolve  rapidly  on  its  long  axis,  as  Para- 
mecium does,  but  usually  creeps  with  its  oral  or  ventral  side  against  a 
surface,  so  that  it  is  not  difficult  to  observe  the  relation  of  the  reaction 
movements  to  the  differences  in  the  sides  of  the  body. 

When  water  containing  a  large  number  of  Oxytrichas  is  placed  in 
the  trough  and  one  end  of  the  trough  is  heated  by  passing  warm  water 
through  the  tube  which  underlies  it,  the  Oxytrichas  gradually  pass 
toward  the  opposite  end  of  the  trough,  forming  a  dense  assemblage 
with  a  rather  sharply  defined  edge  toward  the  heated  side.  If  the  end 
at  first  heated  is  now  cooled  and  the  opposite  end  heated,  the  organisms 
pass  back  to  the  end  from  which  they  first  came.  Similar  results  are 
obtained  by  making  one  end  very  cold ;  the  animals  gather  in  an 
optimum  region,  avoiding  both  too  great  heat  and  too  great  cold.* 
The  phenomena  are  identical  with  what  is  to  be  observed  in  the  case 
of  Paramecium ,  save  that  it  requires  somewhat  longer  for  the  Oxytrichas 
to  move  from  one  end  of  the  trough  to  the  other,  and  the  progress  in  a 
definite  direction  is  not  so  steady  as  we  find  it  in  Paramecium. 

If  the  movements  of  the  individuals  are  observed  we  find  them  to  be 
as  follows :    Near  that   end  of  the  trough  where  the  temperature  is 


♦  Many  quantitative  data  for  various  infusoria  are  given  in  the  valuable  papers 
of  Mendelssohn.  As  the  object  of  the  present  paper  was  not  to  obtain  quantita- 
tive data,  but  to  determine  just  how  the  animals  acted,  absolute  temperatures 
are  not  recorded.  In  every  case  the  experiments  were  so  varied  as  to  use  at 
times  temperatures  to  which  a  reaction  was  hardly  noticeable;  at  other  times 
more  extreme  temperatures,  up  to  those  which  were  destructive. 


i6 


THE    BEHAVIOR   OF    LOWER    ORGANISMS. 


raised  above  the  threshold  vahie  the  animals  begin  to  move  about 
rapidly.  At  first  view  this  movement  seems  to  be  quite  irregular,  as 
Mendelssohn  describes  it  in  Paramecium.     But  exact  observation  of 


Fig.  7.* 

the  individuals  taken  separately  shows  that  this  movement  is  not  so 
entirely  irregular  as  it  at  first  appears.     Most  of  the  animals  swim 

♦Fig.  7.— Method  by  which  Oxytrtcka  fallax  reacts  to  heat  or  cold.  The  fig- 
ure represents  one  end  of  a  trough  or  slide,  which  is  heated  from  the  end  x.  An 
Oxytricha  in  the  position  i  is  reached  by  the  heat  coming  from  the  end  x.     The 


REACTIONS   TO   HEAT   AND    COLD.  1 7 

backward,  circling  at  the  same  time  toward  the  right  or  aboral  side,  as 
shown  in  Fig.  7.  This  lasts  but  a  moment ;  then  the  animal  swims 
forward,  at  the  same  time  turning  to  the  right  or  aboral  side.  That  is, 
the  individuals  give  the  typical  motor  reaction,  as  described  in  the  fifth 
of  my  studies  (Jennings,  1900).  This  reaction  is  repeated  many 
times,  as  long  indeed  as  the  animal  remains  in  the  heated  region.  But 
of  course  this  movement  scatters  the  animals  rapidly.  Those  that 
strike  against  the  end  or  sides  of  the  trough  repeat  the  reaction  above 
described,  backing,  turning  to  the  right,  then  going  forward  (Fig.  7  at 
8,  9,  10,  11).  They  thus  become  directed  in  some  other  way.  Those 
that  are  directed  away  from  the  heated  region  pass  into  cooler  water 
and  hence  no  longer  give  the  reaction,  but  continue  their  course  (Fig. 
7  at  13,  14).  The  result  is  that  the  individuals  which  swim  away  from 
the  heated  end  continue  their  course,  while  those  starting  in  any  other 
direction  are  stopped  and  turned  (through  the  motor  reaction),  until 
they  too  get  started  away  from  the  heated  region.  Thus  after  a  time 
there  is  a  steady  stream  of  organisms  swimming  or  creeping  away  from 
the  heated  end,  while  there  is  no  regular  movement  in  any  other 
direction.  In  this  manner  arises  the  orientation  of  the  animals,  with 
anterior  ends  directed  away  from  the  heated  region. 

The  movements  of  the  individuals  are  exactly  as  above  described 
even  when  the  heat  is  applied  some  distance  from  the  region  where 
the  animal  is  found  and  gradually  approaches  it  from  one  side.  The 
animal  by  no  means  turns  directly  away  from  the  heated  region,  but 
repeatedly  gives  the  backing  and  turning  reaction  till  it  is  finally  mov- 
ing in  a  direction  which  takes  it  out  of  the  heated  region. 

How  is  this  continued  backing  and  turning  to  be  accounted  for  on 
the  theory  of  direct  action  on  the  locomotor  organs  of  the  two  sides  as 
maintained  by  Mendelssohn.?  This  author  speaks  in  the  case  of  Para- 
mecium merely  of  "disordered"  movements  when  the  reaction  first 


animal  reacts  by  turning  to  the  right  and  backing  (i,  2,  3),  turning  again  (3-4), 
swimming  forward  (4-5),  backing  (5-6),  turning  again  to  the  right  ('6-7),  etc., 
till  it  comes  against  the  wall  of  the  trough  (8).  It  then  reacts  as  before,  by 
backing  (8-9),  turning  to  the  right  (9-10).  This  type  of  reaction  continues  as 
long  as  the  Oxytricha  is  in  the  heated  region,  or  as  long  as  its  movements  carry 
it  either  against  the  wall  or  into  the  heated  region.  When  it  finally  becomes 
directed  away  from  the  heated  region  (13),  as  it  must  in  time  if  it  continues  its 
reactions,  it  swims  forward,  and  since  it  is  no  longer  stimulated,  it  no  longer 
reacts.  When  large  numbers  of  animals  react  in  this  way,  in  the  course  of 
time  nearly  all  become  pointed  in  the  same  direction,  as  at  13  or  14,  so  that  a 
marked  "orientation"  is  produced.  Thus  orientation  is  produced  by  "ex- 
clusion," due  to  the  fact  that  the  organism  is  prevented,  either  by  the  heat  or 
the  walls  of  the  trough,  from  swimming  in  any  other  direction. 


l8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

begins,  and  thinks  this  is  due  to  "  individual  differences,  or  to  ill- 
defined  internal  causes,  or  perhaps  rather  to  the  heterogeneity  of  the 
medium  in  which  they  find  themselves"  (Mendelssohn,  1902,  c,  p. 
492),  and  that  it  has  nothing  to  do  with  thermotaxis  proper.  This  is 
typical  of  many  of  the  statements  made  concerning  the  behavior  of  the 
lower  organisms ;  the  movements,  so  long  as  they  do  not  agree  with 
the  preconceived  schema,  are  cast  aside  as  disordered,  and  attention  is 
called  only  to  the  movements  that  do  not  conflict  with  the  theory. 
Thus  Mendelssohn  says  that  this  disordered  movement  ''  ceases  im- 
mediately as  soon  as  the  thermotactic  action  manifests  itself"  (/.  c,  p. 
492).  This  is  true  merely  because  the  thermotactic  action  is  conceived 
to  begin  only  after  the  organism  has,  through  the  movements  above 
described,  gotten  itself  into  such  a  position  that  it  moves  away  from 
the  heated  region.  Of  course  if  all  movements  except  those  after 
orientation  has  occurred  are  thrown  out  of  consideration,  the  orientation 
can  be  accounted  for  in  any  way  desired. 

In  Paramecium,  for  which  alone  Mendelssohn  attempts  to  give  an 
account,  based  on  observation,  of  the  mechanism  of  the  thermotactic 
response,  the  exact  character  of  the  movements  is  undoubtedly  difficult 
to  observe.  This  animal  is  nearly  cylindrical  in  section  ;  the  oral  side 
is  very  slightly  marked,  the  movements  are  rapid,  and  the  animal  con- 
tinually revolves  rapidly  on  its  long  axis,  so  that  observation  of  the 
relation  of  the  direction  of  turning  to  the  differentiations  of  the  body  is 
very  difficult.  In  Oxytricha  and  other  Hypotricha  these  difficulties 
are  almost  absent ;  the  body  is  markedly  differentiated  ;  the  movements 
are  less  rapid,  and,  most  important  of  all,  there  is  usually  no  revolu- 
tion on  the  long  axis.  It  is  unfortunate  therefore  that  Mendelssohn 
included  none  of  the  Hypotricha  among  the  organisms  which  he 
studied.  With  careful  observation  of  the  movements  of  individuals 
the  mechanism  of  the  reactions  is  in  these  animals  absolutely  clear. 

A  crucial  test  of  the  theory  of  direct  orientation  as  maintained  by 
Mendelssohn  is  given  by  observation  of  the  direction  in  which  the 
animals  turn  in  becoming  oriented.  Mendelssohn  (1902,  c,  p.  492) 
says  that  after  the  disordered  movements  ''  the  movements  executed  to 
place  the  body  in  orientation  are  rather  movements  of  rotation."  This 
could  hardly  be  otherwise,  but  the  important  question  for  deciding  as 
to  the  nature  of  the  reaction  is.  How  does  the  rotation  take  place?  Is 
it  determined  by  the  direction  from  which  the  heat  comes,  as  required 
by  Mendelssohn's  theory,  or  is  it  determined  by  the  differentiations  of 
the  animal's  body  }  This  point  is  a  decisive  one  for  interpreting  the 
nature  of  the  reaction.  Suppose  we  have  an  Oxytricha  in  the  position 
a-a,  Fig.  8,  and  heat  is  applied  in  such  a  way  as  to  reach  the  organism 


REACTIONS    TO    HEAT    AND    COLD.  I9 

from  the  direction  indicated  by  the  straight  arrows.    The  heat  is  supra- 
optimal,  so  that  the  organism  moves  away  from  it.     In  what  direction 
will  the  organism  turn  in  order  to  reach  the  position  of  orientation 
h-b'>     According  to  the  theory  of  Mendelssohn,  that  the  orientation 
is  due  to  an  increase  of  the  effective  beat  of  the  cilia  on  the  side  from 
which  the  heat  comes,  the  animal  must  turn  in  the  direction  indicated 
by   the  arrow  x^   and  this   is   of  course    what   one  would  naturally 
expect,  since  this  is  the  most  direct  method  of  becoming   oriented. 
But  as  a  matter  of  fact  the  organism  turns  in  the  opposite  direction,  as 
indicated  by  the  arrow  j)/,  thus  demonstrating  the  incorrectness  of  the 
theory  that  orientation  is  due  to  increase  of  the  effective  beat  of  the 
cilia  on  the  side  from  which  the  heat  comes.     I  have  made  this  obser- 
vation hundreds  of  times,   not  only  upon   Oxytricha,   but  on   other 
Hypotricha  and  on  infu- 
soria belonging  to  other  ,!^ 
groups  (see  below).     The                       ^-'^ ^^^W"^^^ 
direction  of  turning  is  de-                   /       '^  3\  yS^\ 
termined,  under  the  heat               /               '^f  ^^  \ 

stimulus,  by  the  differen-  "If     ^yyy'*^^^  v^l^     ^^   "* ~ 

tiation  of  the    animal's       7)^^^^"^       -^^^-^i  "^^Stz.' -• 

body.     Oxytricha  turns  to         ^^h'<iS^^M'"  •   • '1    o>^  '  ' 

the  right,  without  regard  \V  *^     Z  ^Kv    ^^^^    I!  ^ 

to  the  direction  from  which  ^^\         \^  v\'|)^        /^'      ^         

the  heat  comes.     This  is  \^        %mv        / 

very  striking  when  the  ^'"^^li---"^'' 

trough  is  covered  and  part 

of  the  animals  are  creep-        ^^°-  8.— Method  of  orientation  in  Oxytricha. 

,1  1  .,1  For  details,  see  text. 

mg  on  the  cover-glass  With 

ventral  side  up,  while  the  remainder  are  creeping  on  the  bottom  of  the 
trough  with  ventral  side  down.  When  stimulated  by  heat  approaching 
from  one  side,  all  the  members  of  the  first  group  will  be  9bserved  to 
turn  counter  clock-wise,  while  those  of  the  second  group  turn  in  the 
same  direction  as  the  clock  hands  ;  that  is,  each  specimen  turns  toward 
its  right  side. 

For  becoming  completely  oriented  an  animal  in  the  position  a-a  in 
Fig.  8  usually  requires  a  number  of  reactions,  as  indicated  in  Fig.  7, 
but  the  turning  in  every  case  is  as  indicated  by  the  arrow  j/  (Fig.  8). 

After  it  has  become  oriented  with  the  anterior  end  away  from  the 
source  of  heat,  Oxytricha  by  no  means  maintains  this  position  with 
rigidity  ;  on  the  contrary  the  individuals  shoot  back  and  forth,  in  a  way 
that  might  be  anticipated  from  the  method  in  which  the  reaction 
occurs.     They  thus  form  groups  here  and  there,  which  gradually  move 


20  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

away  from  the  heat,  much  as  is  described  by  Mendelssohn  for  Para- 
mecium bursaria.  With  a  large  number  of  individuals  a  general 
orientation  is  evident,  however,  after  the  experiment  has  been  some 
time  in  progress. 

If  ice  water  is  used  as  the  stimulating  agent  in  place  of  heated  water, 
the  phenomena  to  be  observed  are  practically  identical  with  those 
above  described.  The  organisms  leave  the  colder  region,  giving  the 
same  reaction  as  with  heated  water.  As  the  cold  has  the  additional 
effect  of  decreasing  the  movements,  many  individuals  are  immobilized 
by  a  very  low  temperature  before  they  have  succeeded  in  escaping 
from  it,  so  that  they  remain  in  the  cold  region.  The  reaction  is  thus 
less  clearly  defined  than  that  to  heat. 

Oxytricha  ceruginosa :  This  organism,  though  smaller,  is  in  some 
respects  more  favorable  than  O.  fallax  for  observing  the  method  of 
reaction.  This  is  because  the  individuals  are  more  inclined  to  swim 
freely  through  the  water,  so  that  their  progress  away  from  or  toward 
the  heated  region  is  more  rapid  than  in  O.  fallax.  O.  ceruginosa^ 
further,  even  when  moving  freely  through  the  water,  either  does  not 
revolve  on  the  long  axis  at  all  or  revolves  only  very  slowly.  In  con- 
sequence of  this  it  is  easy  to  determine  the  relation  of  the  direction  of 
turning  to  the  differentiations  of  the  body. 

The  reaction  to  heat  and  cold  is  in  essentials  identical  with  that  of 
O.  fallax,  and  this  reaction  is  repeated  till  the  animals  are  carried  into 
a  region  where  the  temperature  is  not  such  as  to  cause  the  reaction. 
Those  that  are  carried  into  such  a  region  will  of  course  be  swimming 
away  from  the  stimulating  region  ;  hence,  in  a  large  number  of  individ- 
uals there  is  an  evident  orientation,  with  anterior  end  directed  away 
from  the  source  of  heat  or  cold.  All  the  conditions  and  details  as  to 
the  production  of  this  orientation  are  as  set  forth  above  for  O.  fallax. 

Stylonychia  mytilus:  This  large  Hypotrichan  is  still  more  favorable 
for  the  study  of  the  movements  of  individuals  under  the  stimulus  of 
heat  or  cold  coming  from  one  side  than  are  the  two  species  of 
Oxytricha.  But  I  have  found  it  less  easy  to  obtain  in  large  numbers, 
and  for  this  reason  have  not  chosen  it  for  the  detailed  description  of 
the  reaction.  Where  comparatively  few  specimens  are  available, 
the  movements  of  individuals  are  easily  studied,  but  there  is  little 
impression  of  any  real  orientation,  such  as  one  gets  clearly  when  large 
numbers  are  used. 

The  movements  of  the  individuals  are  like  those  described  for 
Oxytricha  fallax.  The  animal  in  reacting  always  turns  to  its  right, 
without  regard  to  the  relation  of  this  to  the  direction  from  which  the 
heat  or  cold  is   coming.     With  an   organism   of  the    large   size   of 


REACTIONS    TO    HEAT    AND    COLD.  21 

Stylonychia  this  is  very  evident.  This  turning  to  the  right  under  the 
stimulus  of  heat  and  cold  in  Stylonychia  has  already  been  described 
by  Putter  (1900),  incidentally  to  his  study  of  the  effect  of  contact 
stimuli  in  this  organism. 

Stentor  cceruleus :  Mendelssohn  includes  in  his  paper  a  note  stat- 
ing that  positive  and  negative  thermotaxis  occur  in  some  species  of 
Stentor,  and  giving  the  optimum  ;  but  he  made  no  study  of  the  mech- 
anism of  the  reactions  in  this  animal.  Had  he  done  so,  it  seems  to  me 
that  he  could  not  have  maintained  his  theory  of  the  way  in  which 
the  reaction  takes  place. 

When  one  end  of  the  trough  is  warmed  the  Stentors  near  that  end 
begin  after  a  few  seconds  to  move  about  more  rapidly.  In  most  cases 
the  movement  is  as  follows :  The  animals  swim  backward  some 
distance,  then  turn  toward  the  right  aboral  side  and  swim  forward 
(the  typical  motor  reaction).  Thus  the  general  effect  is  as  of  an 
irregular  movement  in  all  directions.  Those  individuals  which  swim 
forward  toward  the  other  end  of  the  slide  pass  out  of  the  heated  region  ; 
hence  the  motor  reaction  no  longer  takes  place,  and  the  animals  con- 
tinue to  swim  forward.  Those  which  start  in  any  other  direction  do 
not  escape  from  the  heated  region,  and  therefore  soon  give  again  the 
motor  reaction,  backing  and  turning  again  to  the  right.  Thus  only 
those  that  swim  away  from  the  heated  region  continue  their  course ; 
the  others  are  stopped  and  turned  until  finally  they  too  get  started  in 
the  same  direction.  Therefore,  after  a  period  of  apparently  disordered 
swimming,  there  is  an  evident  orientation  of  many  individuals,  with 
anterior  ends  away  from  the  heated  region.  This  orientation  is  caused 
as  it  were  by  exclusion  ;  in  animals  swimming  in  any  direction  but  one 
the  motor  reaction  is  produced,  so  that  only  this  direction  can  be  main- 
tained. After  a  time,  therefore,  a  large  proportion  of  the  individuals 
are  swimming  in  this  direction,  with  a  common  orientation. 

Thus  the  direction  in  which  the  animals  turn  is  determined,  as  in 
the  Hypotricha,  by  the  structure  of  the  body,  and  not  by  the  direction 
from  which  the  heat  comes. 

Those  outside  the  region  where  the  heat  has  reached  the  threshold 
temperature  often  swim  for  some  distance  toward  the  heated  region ; 
then  arriving  at  a  point  where  the  heat  is  effective,  they  give  the  motor 
reaction,  backing  and  turning  to  the  right.  They  are  thus  prevented 
from  entering  the  heated  region. 

If  the  temperature  is  rapidly  raised,  the  animals  may  not  succeed  in 
escaping  from  the  heated  region  until  they  are  injured.  In  this  case 
the  specimen  contracts  strongly  and  swims  backward  a  long  time.  It 
becomes  distorted,  places  the  disk  against  the  bottom  or  other  surface, 
becomes  motionless,  and  finally  dies. 


ii  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Fixed  specimens  react  less  readily  to  heat  than  do  free-swimming 
specimens.  They  do  not  orient  themselves  with  reference  to  the  direc- 
tion from  which  the  rise  in  temperature  comes.  They  may  remain 
extended  normally,  carrying  on  the  usual  activities,  after  the  tempera- 
ture has  risen  beyond  the  point  which  sets  the  free  specimens  in  rapid 
reaction.  But  as  the  temperature  rises  they  repeatedly  bend  over  into 
a  new  position  (bending  toward  the  right  aboral  side),  then  contract 
strongly,  and  finally  free  themselves  from  their  attachment.  There- 
upon they  behave  like  other  free  individuals. 

Spirostomum  ambiguum :  In  this  large  ciliate  the  reactions  to  heat 
and  cold  take  place  in  essentially  the  same  manner  as  is  described 
above  for  Stentor  and  the  Hypotricha,  so  that  it  is  not  necessary  to 
describe  the  phenomena  in  detail.  The  organism  reacts  to  heat  or 
cold  by  backing  and  turning  toward  its  aboral  side  ;  and  this  whether 
the  change  in  temperature  is  uniform  over  the  entire  surface  of  the 
animal  or  whether  it  approaches  from  one  side.  The  movements  of  the 
animal  are  slow,  and  under  the  Braus-Driiner  stereoscopic  microscope 
its  method  of  reaction  is  very  clear.  There  is  little  marked  common 
orientation  at  any  time,  however  ;  this  being  due  to  the  slowness  of  the 
movements  and  the  frequency  of  repetitions  of  the  motor  reaction. 

Bursaria  truncatella :  In  this  very  large  infusorian,  in  which  cer- 
tain differentiations  of  the  body  are  visible  even  to  the  naked  eye,  the 
method  of  reaction  to  heat  and  cold  is  observed  with  the  greatest  ease. 
But  orientation  of  a  large  number  of  individuals  in  a  common  direction 
is  hardly  to  be  noticed,  though  if  Bursaria  could  be  obtained  in  such 
numbers  as  Paramecium  or  Oxytricha,  perhaps  an  indication  of  orien- 
tation would  be  noticeable  in  spite  of  the  slowness  of  movement. 

Bursaria  is  very  inactive,  often  remaining  quiet  for  long  periods. 
It  swims  slowly,  and  frequently  creeps  along  the  bottom  with  ventral 
side  down,  but  may  also  swim  freely  through  the  water,  revolving  to 
the  left.  If  the  temperature  of  the  trough  is  raised  at  one  end,  the 
animals  in  this  region  that  are  moving  freely  through  the  water  swim 
backward,  turn  to  the  right,  and  swim  forward.  This  may  be  repeated 
till  the  organism  passes  out  of  the  heated  region.  Rather  more 
frequently,  however,  the  animal,  after  thus  reacting  once  or  twice,  sinks 
to  the  bottom  and  places  its  ventral  side  against  the  surface.  It  now 
conducts  itself  in  the  same  manner  as  do  the  other  individuals  in  this 
situation,  as  will  be  described. 

The  individuals  which  are  resting  against  the  bottom  (usually  the 
majority  of  those  in  the  trough)  react  as  follows :  They  begin  to  swim 
backward,  keeping  the  ventral  side  down  and  at  the  same  time  circling 
toward  their  own  right  sides.    They  thus  describe  rather  narrow  circles. 


REACTIONS    TO    HEAT    AND    COLD.  2^ 

This  continues  until  the  heat  becomes  destructive — the  animals  cease 
circling,  become  quiet,  and  finally  disintegrate.  The  reaction  of  those 
individuals  which  are  resting  or  creeping  on  the  bottom  is  thus  not  of 
a  character  to  save  them  from  destruction. 

Specimens  which  are  by  chance  moving  along  the  bottom  from  a 
cool  region  toward  the  warm  region  do  not  escape ;  they  merely  stop 
and  begin  to  circle  backward  to  the  right  when  they  reach  the  heated 
spot,  and  continue  this  till  they  die. 

Thus  the  reaction  of  Bursaria  to  heat,  while  of  the  same  general 
character  as  that  of  other  infusoria,  must  be  accounted  very  imperfect, 
since  it  hardly  results  in  orientation  at  all,  and  does  not  preserve  the 
animals  from  destruction. 

Paramecium  caudatum :  *  In  the  second  of  my  studies  (Jennings, 
1899,  pp.  334-336)  I  gave  a  brief  account  of  the  way  in  which,  ac- 
cording to  my  observations,  Paramecium  reacts  to"  heat  and  cold. 
From  my  more  recent  studies  I  can  confirm  this  account.  But  as 
Mendelssohn  has  recently  come  to  different  conclusions  for  the  tempera- 
ture reaction  of  this  animal,  and  as  he  misunderstands  certain  points 
in  my  brief  description,  it  seems  desirable  that  I  should  supplement  the 
account  previously  given  in  order  to  make  it  clear. 

Paramecium  reacts  to  heat  and  cold  in  essentially  the  same  manner 
as  is  described  above  in  detail  for  Oxytricha.  When  the  higher  or 
the  lower  temperature  advances  from  one  side  the  animals  swim 
backward,  turn  toward  the  aboral  side,  and  swim  forward  again. 
They  continue  this  until  the  movement  brings  them  into  a  region  of 
more  moderate  temperature.  Paramecium  reacts  more  readily  than 
Oxytricha,  the  reactions  are  repeated  at  shorter  intervals,  and  the 
movements  are  more  rapid,  so  that  a  common  orientation  of  many 
individuals  swimming  away  from  the  region  of  higher  or  lower  tem- 
perature is  more  quickly  produced  and  is  more  striking  to  the  eye.  It 
results  farther  from  this  more  rapid  movement,  as  well  as  from  certain 
other  factors,  that  the  method  of  reaction  in  Paramecium  is  much  less 
easily  observed  than  in  any  of  the  other  infusoria  described.  Indeed, 
Paramecium  is  one  of  the  most  unfavorable  forms  obtainable  for  a 
study  of  reaction  methods,  and  it  is,  I  believe,  due  largely  to  the  fact 
that  this  animal  is  usually  employed  for  such  study  that  progress  has 


♦The  common  Paramecium,  which  appears  everywhere  in  immense  numbers 
in  decaying  vegetation,  receives  from  different  authors  sometimes  the  name 
Paramecium  aurelia,  used  by  Mendelssohn ;  sometimes  the  name  given  above. 
I  use  the  name  caudatum  because  it  appears  to  me  to  be  the  correct  one,  but 
there  is  no  reason  for  considering  the  animals  thus  differently  denominated  to 
be  really  different. 


24  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

been  so  slow  in  appreciating  the  real  nature  of  the  reactions  of  the  in- 
fusoria. If  Stylonychia  or  Oxytricha  or  any  other  of  the  Hypotricha 
had  been  taken  as  the  usual  type  for  study  on  reactions,  many  of  the 
theories  now  maintained  could  never  have  been  put  forth.  The  body 
of  Paramecium  is  comparatively  little  differentiated,  so  that  it  is  diffi- 
cult to  distinguish  oral  and  aboral  sides,  and,  to  multiply  tliis  difficulty 
many  times,  the  animal  revolves  rapidly  on  its  long  axis,  so  that  oral 
and  aboral  sides  never  retain  for  two  successive  instants  the  same 
position.  It  is  not  wonderful,  therefore,  that  the  method  of  reaction 
by  turning  toward  the  aboral  side  was  not  observed  in  the  first  investi- 
gations on  Paramecium  and  that  many  still  find  it  difficult  to  observe. 
Nevertheless,  it  was  on  Paramecium  itself  that  this  reaction  method  was 
first  observed  (Jennings,  1S99),  and  its  existence  was  confirmed  later 
on  the  organisms  where  its  observation  presents  no  difficulties.  Aside 
from  the  direct  observations  of  the  method  of  reaction,  the  following 
facts  throw  light  on  the  way  in  which  the  collections  take  place. 

As  described  in  the  second  of  my  studies 
(Jennings,  1899,  pp.  314,  315),  the  collect- 
ing of  Paramecia  in  regions  of  optimum 
temperature  may  be  produced  in  the  follow- 
ing manner  :  The  infusoria  are  mounted  in 
„         ^  water  which  is  above  the  optimum  temper- 

ature (say  30°)  on  a  slide  beneath  a  cover 
glass  supported  at  its  ends  by  glass  rods.  Into  this  slide  is  introduced 
with  the  capillary  pipette  a  little  cooler  water  (say  at  24°),  which 
covers  a  small  circular  area  in  the  center  of  the  slide.  Very  soon  the 
Paramecia  have  collected  in  this  region  till  a  dense  group  is  formed. 
The  same  result  may  be  obtained  by  placing  a  drop  of  ice  water  on  the 
top  of  the  cover  glass  of  a  slide  of  Paramecia  which  has  been  warmed 
considerably  above  the  optimum  temperature.     (Fig.  9.) 

Are  these  collections  due  to  the  orienting  of  Paramecium  by  the 
heat,  as  maintained  by  Mendelssohn  for  thermotaxis  in  general.?  Ob- 
servation shows  that  they  are  not ;  that  on  the  contrary  the  Paramecia 
gather  in  the  optimum  region  in  the  same  manner  as  they  gather  in  a 
drop  of  weak  acid,  as  described  in  my  studies.  The  Paramecia  on  the 
heated  slide  are  swimming  rapidly  in  all  directions.  They  do  not 
change  their  course  or  become  oriented  in  the  least  when  a  spot  in  a 
certain  part  of  the  slide  is  cooled.     But  as  a  consequence   of  their 


*FiG.  9. — Collection  of  Paramecia  due  to  the  reaction  to  temperature  change. 
The  slide  rests  on  a  vessel  of  water  at  a  tetnperature  of  45".  An  elongated  drop 
of  ice  water  is  placed  on  the  upper  surface  of  the  cover  glass.  The  Paramecia 
quickly  collect  beneath  the  drop  of  ice  water. 


REACTIONS    TO    HEAT   AND    COLD.  35 

rapid  movements  many  of  them  by  chance  enter  the  cooler  region. 
They  do  not  react  at  all  as  they  enter,  but  continue  across.  On 
coming  to  the  other  side  of  the  drop,  however,  they  do  react,  by  back- 
ing and  turning  toward  one  side  (the  aboral).  They  react  whenever 
they  come  to  the  boundary  of  the  cooled  region  ;  hence  they  do  not 
leave  it.  In  every  respect  their  behavior  is  like  that  seen  when  Para- 
mecia  collect  in  a  drop  of  weak  acid,  and  I  believe  there  is  no  longer 
anyone  who  holds  to  the  orientation  theory  for  the  gathering  of  Para- 
mecium in  chemicals. 

As  in  the  case  of  chemicals,  it  may  be  demonstrated  to  the  eye  in  the 
following  manner  that  the  method  above  described  suffices  to  account 
for  the  gatherings.  On  the  upper  surface  of  the  cover  glass  is  marked 
a  small  ring  in  ink.  By  confining  the  attention  to  this  ring  it  is  easily 
seen  that  in  the  heated  preparation  of  Paramecia  many  individuals 
cross  the  ring  every  instant,  so  that,  if  these  could  all  be  stopped  in 
the  ring,  a  dense  aggregation  would  soon  result.  Then  the  region 
within  the  ring  is  cooled  by  placing  a  drop  of  ice  water  on  the  cover 
above  it.  The  Paramecia  continue  to  swim  just  as  before,  save  that 
they  no  longer  pass  out  of  the  ring  after  swimming  in,  as  they  did  at 
first.     In  this  way  a  dense  collection  is  soon  formed. 

Mendelssohn  (1902,  ^,  p.  487)  finds  it  inexplicable  why  the  Para- 
mecia should  form  dense  aggregations  at  the  optimum  temperature. 
He  says  that  they  execute  "  only  some  insignificant  movements"  in 
this  region,  not  swimming  away.  On  the  theory  of  thermotaxis  held 
by  Mendelssohn  this  is  perhaps  inexplicable,  but  this,  it  seems  to  me, 
is  only  because  the  theory  is  incorrect.  Such  collections  are  due  to 
precisely  the  same  factors  as  the  rest  of  the  reaction  to  heat  and  cold 
and  are  clearly  intelligible  when  the  nature  of  the  reaction,  as  described 
above,  is  taken  into  consideration.* 

In  a  former  paper  (Jennings,  1S99,  p.  336),  after  giving  a  brief 
account  of  the  reaction  method  above  described,  I  pointed  out  that  this 
method  does  not  demand  a  sensitiveness  to  such  minute  differences  in 
temperature  as  does  Mendelssohn's  theory,  and  that  therefore  the  sensi- 
tiveness  to   temperature    differences    may   have   been   overestimated. 


*  Mendelssohn  (1902,  A,  p.  487)  supposes  that  I  would  explain  these  gatherings 
at  the  optimum  temperature  through  the  collection  of  Paramecia  in  COg  pro- 
duced by  themselves,  and  shows  that  this  would  not  account  for  the  phenomena 
observed  in  these  cases,  though  he  confirms  the  fact  of  the  collections  in  COg. 
But  I  have  by  no  means  maintained  that  such  collections  can  be  produced  only 
by  CO2  ;  on  the  contrary,  I  have  given  an  account  of  many  different  agencies 
that  will  give  rise  to  such  collections,  and  have  especially  described  the  fact  that 
collections  are  formed  in  a  warmed  region  through  exactly  the  same  reacti©n  by 
which  they  are  formed  in  CO^.     (Jennings,  1899,  P*  S^SO 


26  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Mendelssohn  (1902,  a,  p.  406)  misunderstands  my  ground  for  this 
statement.  He  supposes  that  I  hold  that  the  Paramecia  do  not  react 
to  differences  in  temperature  less  than  that  existing  in  a  certain  illus- 
trative experiment,  where  one  end  of  the  slide  was  resting  on  ice,  while 
the  other  was  heated  to  40°.  This  experiment  was  purely  for  the 
purpose  of  bringing  the  phenomena  of  thermotaxis  concretely  before 
the  attention  of  the  reader ;  its  details  had  no  special  significance.  I 
have  not  the  slightest  reason  for  doubting  the  entire  accuracy  of  the 
quantitative  experimental  results  set  forth  by  Mendelssohn,  and  consider 
them  a  most  valuable  addition  to  our  stock  of  exact  data.  But  the 
calculation  of  the  sensitiveness  of  the  organisms  concerned,  from  these 
experimental  results,  involves  a  certain  interpretation  as  to  the  reaction 
method,  and  it  was  this  interpretation  that  I  called  in  question.  Men- 
delssohn, in  accordance  with  his  general  theory,  holds  that  the  reaction 
is  due  to  the  difference  in  temperature  between  the  two 
ends  of  the  organism,  and  he  calculates  that  this  difference 
in  temperature  could  amount,  in  the  case  of  Paramecia, 
to  but  0.01°  C.  According  to  the  reaction  method  which 
I  have  described  above,  however,  it  is  not  the  difference 
in  temperature  between  the  two  ends  of  the  same  indi- 
vidual that  causes  the  reaction.  Consider  a  slide  cooled 
below  the  optimum  at  the  end  a  ;  above  the  optimum  at 
the  end  b  (Fig.  10),  the  optimum  temperature  for  the 
Paramecia  being  between  the  lines  x  and  y.  The  animal 
p  ^  ^  may  swim  a  considerable  distance  from  a  position  y^  at 
one  side  of  the  optimum,  to  a  position  at,  at  the  other  side 
of  the  optimum,  before  it  reacts  (by  backing  and  turning,  etc.)  at  all. 
We  have  no  ground  for  maintaining  then  that  it  perceives  any  less  differ- 
erences  in  temperature  than  that  between  the  lines  x  and  y^  and  this 
difference  will  be  much  greater  than  that  between  the  two  ends  of  the 
animal.  A  similar  diagram  could  be  made  for  the  case  where  the  tem- 
perature is  raised  or  lowered  only  at  one  end  of  the  slide.  It  seems  to 
me  correct,  therefore,  that  the  sensitiveness  to  temperature  differences 
has  probably  been  much  overestimated.  The  only  way  that  it  could 
be  estimated  would  be  by  observation  of  individuals  to  determine  the 
extent  of  the  stretch  x-y  over  which  they  pass  before  reacting,  and  to 
calculate  the  difference  in  temperature  between  the  ends  of  this  stretch. 
It  would  of  course  be  very  difficult  to  do  this  with  accuracy. 

Mendelssohn's  view  that  it  is  the  difference  in  temperature  between 
the  two  ends  of  the  same  individual  that  determines  the  reaction  is  not 


♦  Fig.  id. — Diagram  illustrating  conditions  necessarj'  for  determining  the  sen- 
sitiveness of  Paramecia  to  differences  in  temperature.     See  text. 


REACTIONS    TO    HEAT    AND    COLD.  2*J 

only  rendered  inadmissible  by  the  reaction  method  above  described, 
but  it  is  rendered  a  priori  improbable  by  certain  other  considerations. 
First  we  liave  the  fact  that  the  anterior  end  is  much  more  sensitive  than 
the  posterior.  Of  course  it  is  impossible  to  measure  this  difference  in 
sensitiveness,  yet  the  experiments  with  mechanical  and  chemical  stimuli 
show  that  it  is  great.  In  many  infusoria,  while  the  slightest  touch  at 
the  anterior  end  causes  a  pronounced  reaction,  it  requires  a  strong  stroke 
at  the  posterior  end  to  produce  even  a  slight  reaction.  (See  Jennings, 
1900,  pp.  23S,  243,  251.)  Owing  to  the  much  greater  sensitiveness  of 
the  anterior  end,  it  is  probable  that,  with  the  posterior  end  but  0.01° 
warmer  than  the  anterior,  the  reaction,  if  any,  would  be  due  to  the  tem- 
perature of  the  anterior  end.  In  other  words,  there  is  reason  to  suppose 
that  the  threshold  temperature  for  the  anterior  end  would  be  considera- 
bly lower  than  that  for  the  posterior  end.  If  this  is  true  the  usual  tem- 
perature reactions  would  be  throughout  due  primarily  to  stimulation 
at  the  anterior  end  ;  and  the  reaction,  as  we  have  seen,  is  of  just  the 
character  which  would  be  expected  from  this.  The  first  stage  in 
the  reaction  is  to  swim  backward^  and  this  is  true  also  when  the  animal 
is  dropped  directly  into  water  of  uniformly  high  or  low  temperature,  so 
that  the  temperature  of  the  anterior  end  is  no  greater  than  that  of  the 
posterior  end.  There  is  no  explanation  for  the  swimming  backward 
under  these  circumstances  on  the  theory  that  accounts  for  thermotaxis 
by  the  different  temperature  of  the  two  ends. 

A  second  factor  which  must  be  taken  into  consideration  relates  to  the 
currents  produced  by  the  cilia  of  the  organism  itself.  As  shown  above 
(p.  13) ,  the  water  of  a  higher  temperature  (supposing  that  we  are  deal- 
ing with  the  reaction  to  heat),  would  as  a  rule  first  reach  the  anterior 
end  and  pass  at  once  down  the  oral  groove,  on  the  oral  side  (Fig.  6). 
The  natural  result  therefore  would  be  a  turning  toward  the  opposite  or 
aboral  side,  and  this  is  exactly  what  we  find  takes  place.  We  should 
therefore  not  expect  the  organism  to  turn  directly  away  from  that  end 
of  the  trough  from  which  the  heat  comes,  for  the  heated  water  may  not 
reach  the  Paramecium  from  that  side  at  all. 

As  will  be  seen,  the  facts  adduced  in  the  last  paragraph  are  not  incon- 
sistent with  the  idea  that  the  organism  turns  directly  away  from  the 
side  stimulated.  It  is  the  oral  side  which  is,  as  a  rule,  stimulated,  and 
the  organism  turns  toward  the  aboral  side.  We  seem  thus  to  obtain 
a  most  gratifying  union  of  two  apparently  opposed  views.  But  the 
reactions  to  certain  other  stimuli  do  not  admit  of  such  a  union.  This 
is  notably  true  of  the  reactions  to  mechanical  stimuli,  as  shown  in  a 
previous  paper  (Jennings,  1900),  and  of  the  reactions  to  light,  lo  be 
described  in  the  following  paper. 


a8  THE    BEHAVIOR   OF   LOWER   ORGANISMS. 

SUMMARY. 

The  ciliate  infusoria  react  in  the  same  manner  to  heat  and  cold  as 
to  most  other  classes  of  stimuli ;  the  response  on  coming  into  a  region 
where  the  temperature  is  above  or  below  the  optimum  is  by  backing 
and  turning  toward  a  structurally  defined  side,  followed  by  a  movement 
forward.  This  reaction  is  repeated  as  long  as  an  effective  supraoptimal 
or  suboptimal  temperature  continues.  The  result  is  to  prevent  the 
organisms  from  entering  regions  of  marked  supraoptimal  or  suboptimal 
temperature,  and  to  cause  them  to  form  collections  in  regions  of  opti- 
mal temperature.  The  common  orientation  of  a  large  number  of 
individuals  sometimes  produced  in  this  way  is  an  indirect  result  of  the 
method  of  reaction.  Since  movement  in  any  other  direction  than  a 
certain  one  is  stopped,  the  organisms  after  many  trials  come  into  this 
direction.  Orientation  is  therefore  by  "  exclusion,"  or  by  the  method 
of  trial  and  error.  In  many  of  the  organisms  orientation  is  not  a 
noticeable  feature  of  the  reaction. 


SECOND    PAPER 


REACTIONS  TO  LIGHT  IN  CILIATES 
AND  FLAGELLATES. 


29 


REACTIONS  TO  LIGHT  IN  CILIATES  AND 
FLAGELLATES. 


In  the  reactions  to  light  we  are  dealing  with  a  stimulating  agent 
which  differs  in  one  very  important  respect  from  chemicals  and  from 
heat  or  cold.  The  distribution  of  the  agent  with  which  we  are  con- 
cerned is  not  affected  by  the  currents  of  water  produced  by  the  organism  ; 
hence  there  is  no  tendency  for  one  side  or  part  of  the  organism  to  be 
more  strongly  affected  than  the  rest,  as  was  found  to  be  the  case  for 
chemicals  and  for  heat  and  cold.  This  peculiarity  light  shares  with 
the  electric  current  and  with  radiant  heat.  The  conditions  demanded 
for  immediate  orientation  through  direct  action  of  the  agent  on  the 
locomotor  organs,  in  the  manner  required  by  the  general  theory  of 
tropisms  as  set  forth  in  the  foregoing  paper  (p.  7) ,  are  therefore  present. 
In  a  recent  paper  Holt  &  Lee  (1901)  have  attempted  to  show  that 
the  reactions  of  organisms  to  light  actually  take  place  in  accordance 
with  this  theory. 

We  shall  examine  the  reactions  to  light  in  Stentor  cceruleus  and  in 
certain  flagellates,  in  order  to  determine  whether  they  take  place  in 
accordance  with  the  tropism  schema,  and,  if  not,  just  how  they  do  occur 
and  on  what  factors  they  depend. 

THE  CILIATA. 

STENTOR  C^RULEUS. 

As  is  well  known,  very  few  of  the  ciliate  infusoria  react  to  light. 
Light  reactions  have  been  described  by  Engelmann  (1882,  a)  for  several 
chlorophyllaceous  ciliates  ;  by  Verworn  (18S9,  Nachschrift)  for  Pleuro- 
nema  chrysalis;  and  by  Davenport  (1897)  and  Holt  &  Lee  (1901)  for 
Stentor  cceruleus.  In  none  of  the  ciliates  have  the  reactions  been 
described  in  sufficient  detail  to  enable  us  to  determine  their  exact 
nature. 

In  Stentor  cceruleus  the  reaction  to  light  manifests  itself  in  the 
culture  dish  by  the  usual  aggregation  of  the  organisms  at  the  side  away 
from  the  window.  If  a  number  of  Stentors  are  removed  to  a  watch 
glass  or  trough,  and  this  is  placed  near  a  window  or  other  source  of 
light,  most  of  the  Stentors  are  soon  found  on  the  side  of  the  vessel  away 
from  the  light.     If  one-half  of  the  glass  is  shaded  by  a  screen,  most  of 

31 


32  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

the  Stentors  are  soon  found  in  the  shaded  half.  ^S.  cceruleus  thus  shows 
the  phenomenon  usually  called  negative  phototaxis. 

It  is  to  be  noted  that  not  all  the  Stentors  are  to  be  found  on  the  side 
away  from  the  light,  or  in  the  shaded  half  of  the  vessel.  On  the  con- 
trary, a  considerable  fraction  of  the  whole  number  will  usually  be  found 
swimming  about  in  all  parts  of  the  dish,  or  at  rest  in  the  lighted  portion. 
The  light  reaction  is  thus  somewhat  inconstant,  and  varies  among 
different  individuals.  It  varies  considerably  with  Stentors  of  different 
cultures ;  from  some  cultures  almost  all  the  individuals  show  it,  while 
from  others  it  is  barely  noticeable.  This  variability  and  inconstancy 
run  through  all  manifestations  of  the  light  reaction  in  Stentor. 

A  word  further  needs  to  be  said  as  to  the  behavior  of  individuals 
which  are  not  free-swimming,  but  are  fixed  by  the  posterior  end.  Such 
individuals  do  not  react  at  all  to  light.  When  light  is  thrown  on  them 
they  remain  in  the  positions  in  which  they  are  found  at  the  beginning, 
neither  contracting  nor  in  any  way  changing  their  position.  No  matter 
whether  the  light  is  weak  or  strong,  and  without  regard  to  the  direction 
from  which  it  comes,  fixed  Stentors  give  no  reaction  and  show  no 
orientation  with  reference  to  light.  The  contact  reaction  apparently 
inhibits  the  light  reaction  completely.  We  shall  therefore  omit  the 
fixed  individuals  from  consideration  in  the  remainder  of  the  account, 
confining  attention  to  the  free-swimming  specimens. 

The  typical  motor  reaction  of  Stentor,  by  which  it  responds  to  most 
stimuli,  is  as  follows :  The  Stentor  stops  or  swims  backward  a  short 
distance,  then  turns  toward  the  right  aboral  side,  and  resumes  its  for- 
ward motion.  This  is  the  reaction  which  is  produced  by  strong 
mechanical  stimuli,  by  heat,  and  by  chemical  stimuli,  acting  upon  the 
anterior  end  or  upon  the  body  as  a  whole. 

How  is  the  reaction  to  light  brought  about.?  To  answer  this  ques- 
tion it  is  best  to  arrange  experiments  in  such  a  way  as  to  distinguish 
as  far  as  possible  the  effect  due  to  unequal  illumination  of  different 
areas  from  the  effect  due  to  the  direction  from  which  the  light  is  coming. 

In  order  to  produce  strong  differences  in  illumination  in  different 
areas  of  the  space  in  which  the  Stentors  are  found,  a  flat-bottomed 
glass  vessel  containing  many  Stentors  in  a  shallow  layer  of  water  was 
placed  on  the  stage  of  the  microscope,  in  a  dark  room.  From  beneath 
strong  light  was  sent  upward  through  the  opening  of  the  diaphragm, 
by  throwing  the  light  from  the  projection  lantern  (using  the  electric 
arc  light)  on  the  substage  mirror.  By  this  the  light  was  directed  up- 
ward through  the  vessel  containing  the  Stentors.  Thus  a  small, 
definitely  bounded  circular  area  was  illuminated,  while  the  rest  of  the 
vessel  remained  in  darkness.  A  black  screen  was  usually  placed  over 
the  diaphragm  opening  of  the  microscope  in  such  a  way  as  to  shade  one- 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


33 


half  of  the  circular  area,  making  a  sharp  line  {x-y,  Fig.  ii)  dividing  the 
light  from  the  darkness.  A  mirror  was  placed  above  the  microscope, 
inclined  in  such  a  position  as  to  project  the  image  of  the  Stentors,  very 
much  magnified,  on  the  ordinary  vertical  screen  used  for  receiving 
lantern  slide  views.  Thus  the  behavior  of  the  Stentors  could  be  studied 
with  great  ease  on  the  screen. 

The  heat  from  the  lantern  was  cut  out,  so  far  as  possible,  by  placing 
between  it  and  the  mirror  of  the  microscope  a  glass  cell  three  inches 
thick,  filled  with  cold  water.  In  this  manner  the  heat  was  excluded  to 
such  an  extent  as  to  fall  below  the  threshold  for  the  stimulation  of 
Stentor  by  heat.  This  was  demonstrated  by  comparing  the  reactions 
of  Stentor  with  those  of  Paramecium.  Stentor  is  less  sensitive  to 
changes  in  temperature  than  is  Paramecium  ;  this  was  clear  in  my  ex- 
periments on  the  reaction  to  heat.  Par- 
amecium does  not  react  at  all  on  passing 
into  the  area  illuminated  by  the  lantern, 
but  swims  about  indifferently  in  both  the 
dark  and  the  light  parts  of  the  dish,  show- 
ing that  the  heat  produced  is  below  the 
threshold  for  Paramecium  ;  it  must  then 
be  below  the  threshold  for  Stentor. 

The  free  Stentors  in  the  unlighted  part 
of  the  vessel  swim  about  at  random. 
Many  individuals  thus  come  by  chance  to 
the  line  x-y,  Fig*.  1 1 ,  where  they  would 
pass  into  the  lighted  area.  These  at 
once  back  a  little,  then  turn  toward  the 
right   aboral    side,   and    swim   forward 

again.  The  turning  toward  the  right  aboral  side  is  usually  through  an 
angle  sufficient  to  direct  the  Stentor  away  from  the  lighted  area  (see 
I,  2,  3,  4,  Fig.  ii)  ;  if  it  is  not,  the  Stentor  repeats  the  reaction  until, 
after  one  or  two  trials,  it  swims  into  the  unlighted  region. 

Many  of  the  individuals  react  as  soon  as  the  anterior  end  reaches  the 
lighted  area,  so  that  less  than  one-fourth  of  the  body  is  in  the  light. 
This  shows  that  light  falling  upon  the  anterior  end  alone  is  sufficient 
to  cause  the  reaction. 

A  few  specimens  swim  completely  into  the  lighted  area,  then  react 


♦Fig.  II. — Method  of  studying  the  manner  in  which  Stentor  reacts  to  light. 
The  figure  shows  a  circular  area,  illuminated  from  below,  with  the  light  cut  oft 
from  the  left  side  by  a  dark  screen,  the  line  x-y  separating  the  light  from  the 
dark  area.  The  Stentors  collect  in  the  dark  area.  The  reaction  of  a  specimen 
which  comes  to  ihe  line  x-y  is  shown  at  i,  2,  3,  4. 


34  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

in  the  manner  above  described.  In  such  cases  the  nature  of  the  reac- 
tion is  seen  with  especial  clearness,  the  entire  animal  being  projected 
on  the  screen  and  the  differentiations  of  bodily  structure  (mouth,  oral 
and  aboral  sides,  etc.)  being  conspicuous.  Specimens  which  swim 
completely  into  the  lighted  area  are  usually  compelled  to  react  two  or 
more  times  before  they  escape  from  the  lighted  region. 

When  the  light  is  cut  off  entirely  the  Stentors  distribute  themselves 
throughout  the  dish.  If  the  light  is  now  admitted  from  below,  the 
unattached  Stentors  in  the  lighted  area  react  by  swimming  backwards 
a  certain  distance,  turning  toward  the  right  aboral  side,  then  swimming 
forward  again.  This  reaction  is  repeated  frequently  until  after  an 
interval  the  Stentors  are  carried  by  these  movements  outside  the  lighted 
area.  They  then  cease  to  give  the  reaction.  The  reaction,  under  these 
conditions,  is  thus  the  same  as  that  produced  when  Stentors  or  Para- 
mecia  are  subjected  to  other  adequate  stimuli,  as  when  they  are  placed 
in  a  chemical  or  dropped  into  very  warm  or  very  cold  water.  The 
result  of  the  reaction  is,  in  every  case,  to  remove  the  organism  from 
the  sphere  of  action  of  the  stimulus.  When  the  stimulus  is  light  this 
result  is  produced  in  exactly  the  same  way  as  when  the  stimulus  is 
heat  or  cold  or  a  chemical. 

The  same  results  may  be  obtained  by  lighting  the  vessel  containing 
the  Stentors  directly  from  above  and  shading  one  portion  with  a  screen. 
The  Stentors  remain  in  the  shaded  region,  responding  by  the  motor 
reaction  above  described  when  they  come  to  the  lighted  area.  With  a 
favorable  culture  the  experiment  succeeds  even  when  the  source  of 
light  is  comparatively  feeble,  as  when  an  ordinary  incandescent  electric 
light  is  used  as  the  source  of  illumination. 

The  results  so  far  show  that  a  sudden  increase  in  the  intensity  of 
illumination  induces  in  Stentor  a  reaction  which  is  of  the  same 
character  as  the  reaction  to  other  strong  stimuli.  Such  a  sudden 
increase  may  be  due  either  to  the  passage  of  the  Stentor  from  a  dark 
to  a  light  region,  or  to  a  sudden  increase  in  the  brightness  of  the  light 
which  falls  upon  the  animal.  The  general  effect  of  the  reaction  is  to 
prevent  the  Stentor  from  entering  a  brightly  illuminated  area,  or  to 
remove  it  from  such  an  area. 

We  may  now  arrange  the  conditions  so  that  the  light  shall  come 
from  one  side,  while  at  the  same  time  differences  in  illumination  shall 
exist  in  different  regions.  This  may  be  done  by  illuminating  the  vessel 
containing  the  Stentors  from  the  side,  then  covering  one  portion  of  the 
vessel  with  a  screen. 

The  organisms  are  placed  before  a  lighted  window,  or  an  incandes- 
cent electric  light,  in  a  vessel  with  a  plane  front  (Fig.  12).      One-half 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


35 


of  the  vessel  is  then  cut  off  from  the  light  by  a  screen  (j),  the  shadow 
of  which  passes  across  the  middle  of  the  vessel  containing  the  Stentors. 
One  side  of  the  vessel  is  thus  in  the  light,  the  other  in  the  shadow, 
and  these  two  regions  are  separated  by  a  sharp  line  (Fig.  12,  x  y). 

The  Stentors  are  soon  all  collected  in  the  shaded  side  of  the  vessel. 
Here  they  swim  about  freely  in  all  directions,  but  do  not  cross  the  line 
into  the  lighted  portion.  Now,  by  focusing  the  Braus-Driiner  on  this 
line,  the  behavior  of  the  individuals  on  reaching  it  may  be  observed. 

It  is  well  to  examine 

the  conditions  in  this  case > 

with  care,  as  they  present 
opportunities  for  a  pre- 
cise and  crucial  test  of 
the  theory  that  the  reac- 
tion to  light  is  due  to  a  di-    ^ 

rect  orientation  through 
the  falling  of  light  on  one 
side  of  the  organism  (pho- 
totaxis  or   phototropism 

in  the  strict  sense,  as  de-    * 

fined  by  Holt  &  Lee). 
In  the  lighted  portion  of 
the  vessel  the  rays  of  light 
come  from  a  certain  direc- 
tion, as  indicated  by  the  *" 
large  arrows   (Fig.   12). 

In  the  shaded  region  there     ^ 

is  not  enough  light  to  pro- 
duce orientation,  the  ani- 
mals swimming  in  every  *" 
direction.     On  passing 
from    the   shaded  region 

across  the  line  x-y  into  the  lighted  region,  the  animal  should  (according 
to  the  tropism  theory)  become  oriented.  According  to  the  theory  of 
negative  phototaxis  by  direct  orientation  due  to  differential  action  on 


Fig.  12.* 


*  Fig.  12. — Method  of  testing  the  manner  of  reaction  to  light  in  Stentor.  The 
large  arrows  show  the  direction  from  which  the  light  rajs  come.  A  screen  (s) 
cuts  off  the  light  from  half  the  vessel,  leaving  a  line  (x-y)  separating  a  shaded  part 
from  a  lighted  part.  The  Stentors  collect  in  the  shaded  part,  here  swimming 
about  without  orientation.  At  a  (i,  2,  3,  4)  we  see  a  diagram  of  the  reaction 
required  by  the  tropism  schema  when  the  organism  swims  across  the  line  x-y, 
while  at  d  (i,  2,  3,  4)  we  have  a  diagram  of  the  reaction  as  actually  given  under 
these  conditions. 


^6  THE    BEHAVIOR    OF    LOWER    ORGANIf?MS. 

the  two  sides,  the  animals  on  crossing  the  line  should  become  oriented 
by  turning  directly  away  from  the  source  of  light,  as  shown  in  the 
diagram  (Fig.  12)  at  a.  The  animal  would  then  be  expected  to  swim 
in  the  direction  x-y  as  shown  by  the  specimen  «,  i,  2,  3,  4. 

It  cannot  be  held  that  the  real  source  of  light  for  the  Stentors  is  that 
reflected  from  the  bottom  or  sides  of  the  dish  in  the  lighted  region,  and 
hence  coming  on  the  whole  from  a  direction  perpendicular  to  the  line 
xy^  for  the  behavior  of  the  Stentors  shows  that  this  is  not  the  case. 
A  Stentor  in  the  shaded  region,  close  to  the  line  x-y^  as  at  c.  Fig.  12, 
receives  whatever  light  there  may  be  thus  reflected  exactly  as  it  does 
after  it  has  crossed  the  line,  yet  it  shows  no  reaction  and  does  not 
orient  itself  in  any  way.  On  the  other  hand,  as  soon  as  it  crosses  the 
line  x-y.,  so  as  to  receive  the  light  coming  from  the  window,  it  reacts 
strongly,  as  we  shall  see.  It  is  thus  clearly  the  light  from  the  window, 
coming  in  the  direction  shown  by  the  large  arrows,  that  causes  the  re- 
action ;  hence  the  Stentor  ought,  according  to  the  direct  orientation 
theory,  to  orient  itself  in  the  line  of  these  rays. 

When  a  Stentor,  swimming  at  random,  reaches  the  line  a:-j/,  it 
reacts  by  stopping  suddenly,  then  turning  toward  its  aboral  side, 
then  swimming  forward.  It  thus  swims  about  until  its  anterior  end  is 
again  within  the  shadow,  where  it  continues  to  swim  forward  (Fig.  12, 
3,  1,2,  3,  4).  Often  the  first  reaction  is  not  sufficient  to  direct  it  into 
the  shadow  ;  in  this  case  the  reaction  is  repeated  ;  one  to  three  reactions 
almost  invariably  bring  the  Stentor  back  into  the  shadow.  It  has  no 
particular  orientation  in  the  shadow,  but  swims  in  whatever  direction 
it  happens  to  be  headed. 

Very  frequently  the  animals  react  when  the  anterior  end  alone  has 
crossed  the  line,  so  that  less  than  the  anterior  half  of  the  body  is  lighted. 
In  other  cases  the  animal  swims  completely  across  the  line,  sometimes 
for  a  distance  greater  than  its  own  length,  into  the  light,  before  it  reacts. 
In  any  case  the  reaction  is  that  above  described. 

Does  the  Stentor,  when  it  turns  on  entering  the  light,  always  turn 
away  from  the  source  of  light,  as  the  theory  of  direct  orientation 
requires  .'' 

At  the  moment  of  crossing  the  line  into  the  light  the  »Stentor  may 
occupy  various  positions.  It  will  be  well  to  note  specifically  the  re- 
action in  certain  of  these  positions,  as  we  obtain  here  the  observations 
which  furnish  an  exact  and  crucial  test  of  the  direct  orientation  theory. 

I.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed 
toward  the  source  of  light  (Fig  12,  b).  It  therefore  turns  (as  usual) 
toward  its  aboral  side.  It  thus  swings  its  anterior  end  toward  the 
source  of  lights  in  the  direction  opposite  that  required  by  the  direct 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


37 


orientation  theory.  This  observation  was  made  repeatedly  in  a  very 
large  number  of  cases  ;  not  a  single  exception  to  it  was  observed.  The 
swinging  of  the  anterior  end  is  continued  past  the  point  where  the  light 
falls  directly  upon  it  until  the  animal  is  directed  again  into  the  shadow, 
as  illustrated  in  the  diagram  (Fig.  12,  ^,  i,  3,  3,  4). 

2.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed  away 
from  the  source  of  light.  In  this  case  it  turns  (as  usual)  toward  the 
aboral  side,  thus  swinging  its  anterior  end  away  from  the  source  of  light. 

3.  The  Stentor  may  reach  the  line  with  the  aboral  side  directed 
upward  or  downward  or  in  some  intermediate  position.  In  every  case 
it  turns  toward  the  right  aboral  side,  in  whichever  way  this  is  directed. 


The  writer  wishes  it  to  be  understood  that  the  foregoing  statements 
as  to  the  direction  in  which  the  animal  turns  are  presented,  not  merely 
as  interpretations  in  accordance  with  a  certain  theory,  but  as  direct, 
unequivocal  observations,  many  times  repeated.  Thus,  on  passing  from 
a  darker  to  a  lighter  area,  even  when  the  light  comes  from  one  side, 
the  Stentors  react  merely  to  the  difference  in  illumination,  without 
regard  to  the  direction  from  which  the  light  comes.  The  direction  of 
turning  is  determined  tln-oughout  by  an  internal  factor,  not  by  the  side 
of  the  animal  on  which  the  light  falls,  nor  by  the  direction  of  the  rays  of 
light.     We  have  put  the  theory  of  orientation  by  direct  differential 


♦Fig.  13. — Another  method  of  testing  the  manner  in  which  Stantor  reacts  to 
light.  For  a  side  view  of  this  apparatus,  see  Fig.  14.  Light  comes  from  the 
left  side,  in  the  direction  indicated  by  the  arrows.  A  screen  (5)  is  interposed 
between  the  source  of  light  and  the  vessel  containing  the  Stentors.  This  screen 
is  of  such  a  height  (as  illustrated  in  Fig.  14)  that  it  cuts  off  the  light  from  the 
half  (/4)  of  the  vessel  next  to  the  window,  leaving  the  other  half  {B)  lighted. 
At  c  (i,  2,  3,  4,  5)  is  seen  the  reaction  method  of  a  specimen  which  swims  across 
the  line  x-y,  separating  the  shaded  half  ^  from  the  lighted  half  ^. 


3S 


THE    BEHAVIOR    OF    LOWER    ORGANISMS, 


action  of  the  light  on  the  two  sides  of  the  animal  to  a  precise  test,  and 
found  it  to  be  incorrect. 

The  same  result  is  brought  out  in  perhaps  a  still  more  striking 
manner  by  the  following  method  of  experimentation :  A  vessel  con- 
taining Stentors  is  placed  on  a  dark  background  near  a  source  of  light 
(a  window  or  an  incandescent  electric  lamp).  The  light  thus  comes 
from  one  side  and  a  little  from  above.  An  opaque  screen  is  placed 
between  the  window  and  the  vessel  containing  the  Stentors,  of  such  a 
size  and  in  such  a  position  that  the  top  of  the  shadow  of  the  screen  falls 
across  the  middle  of  the  vessel  on  the  line  x-y  (Fig.  13  ;  see  also  Fig. 
14).  Thus  the  half  of  the  vessel  next  to  the  window  (-4)  is  darker 
than  the  farther  half  (-5),  and  the  Stentors  collect  in  this  shaded  half 
After  some  time  scarcely  a  specimen  is  found  in  the  lighted  part  of  the 
vessel  away  from  the  window.  The  conditions  in  this  case  are  illus- 
trated in  the  side  view  (Fig.  14). 

The  exact  behavior  of  the  Stentors  in 
the  darkened  portion  of  the  vessel  is  then 
studied  by  focusing  upon  them  the  Braus- 
Driiner  microscope.  The  Stentors  within 
the  shaded  area  are  not  oriented  nor  gath- 
ered in  any  particular  region, 
but  swim  about  at  random. 
When  one  of  the  specimens 
comes  in  its  course  to  the 
line  :v-j/ (Fig.  13),  separating 
the  darkened  area  from  the 
light,  it  responds  to  the  sudden  light  which  falls  upon  it  from  the 
window  by  giving  the  motor  reaction,  turning  to  the  right  aboral  side 
and  swimming  back  into  the  shaded  region.  Often  the  reaction  occurs 
as  soon  as  the  anterior  end  of  the  Stentor  has  crossed  the  line  x-y^  so 
that  the  entire  Stentor  does  not  pass  out  into  the  lighted  area.  In  other 
cases  the  specimen  crosses  the  line  x-y  completely  before  the  reaction 
occurs,  so  that  the  entire  body  is  illuminated.  It  then  reacts  in  the 
usual  manner,  turning  toward  the  right  aboral  side,  so  that  it  is  headed 
toward  the  shaded  region ;  thus  swimming  back  across  the  line  (Fig. 
13,  c) .  After  returning  into  the  shaded  region  the  animals  swim  about 
at  random  as  before. 

What  is  the  reason  for  the  return  of  the  Stentor  into  the  darkened 
area  after  it  has  crossed  the  line  into  the  light  region.? 


♦Fig.  14. — Sectional  view,  from  the  side,  of  the  conditions  shown  in  Fig.  13. 
The  arrows  show  the  direction  of  the  light  rays.  The  region  from  5  to  ;«  is 
shaded  by  the  screen  s. 


REACTIONS   TO    LIGHT    IN   CILIATES    AND    FLAGELLATES.  39 

By  SO  doing  it  swims  toward  tlie  window,  thus  in  the  direction  from 
which  the  strongest  light  is  coming.  According  to  the  theory  of  photo- 
taxis  as  due  to  the  direct  action  of  the  light  on  the  motor  organs  of  the 
animal,  this  movement  is  inexplicable.  Thus,  in  the  analysis  of  this 
theory  given  by  Holt  &  Lee  (1901),  it  is  shown  that  in  the  case  of  a 
negative  organism,  such  as  Stentor,  light  of  supraoptimal  intensity, 
like  that  coming  from  the  window,  must  be  assumed  to  cause  increased 
contraction  of  the  cilia.  After  the  organism  has  passed  across  the  line 
x-y,  or  while  it  is  passing  across  this  line,  it  has  the  anterior  end  directed 
away  from  the  source  of  light ;  according  to  the  tropism  theory  this 
is  a  stable  position  and  should  not  be  changed.  For,  supposing  the 
organism  swerves  a  little  toward  either  side,  the  cilia  on  that  side  will 
be  more  strongly  affected  by  the  light,  so  that  the  animal  will  at  once 
be  turned  back  into  the  position  of  equilibrium  with  anterior  end  directed 
away  from  the  light. 

Nevertheless,  under  these  circumstances  the  organism  does  turn  and 
swim  back  into  the  darkened  area.  An  explanation  for  the  apparent 
movement  of  a  negative  organism  against  the  direction  of  the  light  rays 
is  sometimes  given  in  the  following  form  :  The  light  from  the  window 
is  said  to  fall  upon  the  side  or  end  of  the  dish  farthest  from  the  window 
and  is  reflected  back,  so  that  the  chief  source  of  light  for  the  Stentors 
is  not  the  window,  but  the  side  of  the  dish  opposite  the  window.  The 
animal  therefore  becomes  oriented  with  relation  to  this  source  of  light 
and  swims  away  from  it. 

Comparison  of  the  movements  of  the  Stentors  in  the  darkened  area 
A  with  those  in  the  lighted  area  B  shows  that  this  explanation  can  not 
possibly  be  correct.  Consider  an  individual  at  the  point  <5,  Fig.  13, 
which  turns  and  swims  toward  the  window  into  the  dark  region.  It 
is  affected  by  light  from  two  sources,  (i)  from  the  window,  (2)  reflected 
from  the  side  opposite  the  window.  According  to  the  above  theory 
the  turning  is  due  to  the  fact  that  the  light  from  the  opposite  side  is  of 
greater  strength  than  that  from  the  window  (in  itself  a  most  improbable 
suggestion).  Compare  this  Stentor  b  with  an  individual  at  at,  in  the 
darker  region.  This  animal  receives  no  direct  rays  from  the  window, 
yet  does  receive  the  reflected  rays  from  the  opposite  side.  If  these 
reflected  rays  are  sufficient  to  cause  b  to  become  oriented  in  spite  of 
the  opposing  rays  from  the  window,  they  must  produce  the  same  effect, 
a  fortiori^  on  the  individual  «,  since  they  are  the  only  rays  which 
reach  it  Yet  individuals  in  the  position  a  do  not  become  oriented  at 
all.  The  individuals  in  the  shaded  portion  of  the  vessel  swim  about 
in  all  directions,  without  relation  to  the  direction  of  the  light  rays.  It 
is  only  when  they  come  to  the  line  x-y.^  where  they  would  pass  into  the 


40  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

region  lighted  directly  from  the  window,  that  they  react  by  turning 
toward  the  right  aboral  side  and  passing  back  into  the  shadow.  It  is 
thus  clear  that  it  is  the  light  coming  from  the  window  to  which  they 
react,  not  the  light  reflected  from  the  sides  of  the  dish.  We  have  here 
realized  the  condition  concerning  which  there  has  been  so  much  dis- 
cussion, and  which  has  been  considered  impossible  and  unrealizable  by 
various  authors — a  negative  organism  reaching  the  darker  region  by 
swimming  toward  the  source  of  strongest  light. 

This  would  of  course  be  quite  inexplicable  on  the  tropism  theory  as 
set  forth  by  Holt  &  Lee.  What  does  it  indicate  as  to  the  real  nature 
of  the  reaction?  To  this  inquiry  there  can  be  but  one  answer.  The 
organism  reacts  on  passing  from  a  darker  to  a  lighter  area,  without 
regard  to  the  direction  from  wliich  the  light  comes.  It  reacts  to  the 
increase  in  the  amount  of  light  falling  upon  it  as  compared  with  the 
condition  an  instant  before  it  had  passed  into  the  lighted  area.  The 
reaction  takes  the  usual  form — a  backing  and  turning  toward  the  right 
aboral  side,  followed  by  a  forward  motion.  The  organism,  therefore, 
is  directed  again  toward  the  shaded  area,  which  it  enters. 

In  all  our  experiments  thus  far  there  have  been  marked  differences 
in  the  illumination  of  different  areas.  Let  us  now  arrange  the  condi- 
tions so  that  light  comes  from  one  side,  and  all  parts  of  the  vessel  are 
equally  illuminated.  This  may  be  done  by  placing  the  Stentors  in  a 
glass  vessel  with  plane  walls  at  one  side  of  a  source  of  light,  such  as  a 
window  or  the  bulb  of  an  incandescent  electric  light.  The  Stentors, 
after  a  very  short  interval  in  which  the  reaction  seems  indefinite,  swim 
away  from  the  source  of  light,  thus  gathering  at  the  side  away  from 
the  window,  where  they  move  about  in  a  disordered  way.  During  the 
reaction  the  Stentors  are  oriented^  with  the  longitudinal  axis  in  the 
general  direction  of  the  light  rays  and  with  the  anterior  end  away  from 
the  source  of  light. 

Thus  while  it  is  true  that  the  direction  of  the  rays  of  light  has  little 
if  any  effect  on  the  reaction  when  the  animals  are  at  the  same  time 
subjected  to  a  sudden  change  from  dark  to  light,  it  does  determine  the 
direction  of  movement  when  acting  alone.  In  order  to  discover  just 
how  the  reaction  occurs  it  is  necessary  to  observe  the  animals  at  the 
moment  when  they  change  from  their  former  undirected  swimming  to 
the  movement  away  from  the  source  of  light. 

For  determining  this  a  large  number  of  Stentors  are  placed  in  the 
dish  next  the  window  on  a  dark  background.  The  light  comes  from 
one  side  and  a  little  from  above.  The  direct  rays  of  the  sun  were  not 
employed. 

Above  the  glass  vessel  are  focused  the  lenses  of  the  Braus-Driiner 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  4I 

stereoscopic  binocular.  This  gives  a  magnification  of  6^  diameters, 
with  a  working  distance  of  3  cm.,  and  permits  exact  observation  of 
the  movements  of  the  individual  Stentors.  To  one  who  has  worked 
only  with  the  monocular  microscope,  the  use  of  the  stereoscopic  binocu- 
lar in  studying  the  movements  of  small  organisms  will  be  a  revelation. 

The  vessel  containing  the  Stentors  is  first  covered  with  a  dark  screen 
and  the  Stentors  are  allowed  to  become  equally  distributed  throughout 
the  dish.  The  screen  is  then  raised,  allowing  the  light  from  the  window 
to  fall  upon  the  Stentors.  Those  which  are  swimming  in  any  other 
direction  than  away  from  the  window  now  turn  and  in  a  short  time 
are  swimming  toward  the  side  of  the  dish  away  from  the  window. 

With  the  Braus-Driiner  the  movements  of  individuals  are  observed 
at  the  moment  of  removing  the  screen.  Some  turn  at  once,  while  most 
continue  for  a  few  seconds  in  the  direction  in  which  they  are  swimming 
and  then  turn.  All  turn  in  every  case  toward  the  right  aboral  side. 
The  turning  is  continued  or  repeated  until  the  anterior  end  is  directed 


tes 


Fig.  15.* 

away  from  the  window  ;  then  the  direct  course  is  continued,  carrying  the 
Stentor  to  the  side  of  the  dish  away  from  the  window.  The  direction 
of  tur7iing  is  thus  determined  by  an  internal  factor — the  structure 
of  the  body. 

The  behavior  of  the  Stentors  may  be  controlled  and  studied  more 
exactly  by  a  diflferent  order  of  experimentation.  The  animals  are 
placed  in  a  shallow  rectangular  glass  vessel  on  a  dark  background,  in 
a  room  that  is  entirely  dark  save  for  two  incandescent  electric  lights 
A  and  B  (Fig.  15).  These  are  clamped  in  position,  one  on  each  side 
of  the  dish  containing  the  Stentors,  and  about  eight  inches  from  it. 
Both  these  lights  can  be  turned  on  at  once ;  both  can  be  extinguished 
or  one  can  be  turned  on  while  the  other  is  turned  off.  When  only  one 
is  turned  on  the  direction  of  the  light  can  be  instantly  reversed  by 
simultaneously  extinguishing  this  one  and  turning  on  the  other. 

With  both  lights  extinguished  the  Stentors  in  the  vessel  are  allowed 
to  become  equally  distributed  ;  then  B  is  illuminated.     In  a  short  time 


♦Fig.  15. — Method  of  testing  the  reaction  of  Stentor  to  light.     A  and  B  are 
incandescent  electric  lights. 


42  THE    BEHAVIOR    OP    LOWER    ORGANISMS. 

most  of  the  individuals  have  gathered  at  the  side  next  to  A^  as  in 
Fig.  15.  Then  B  is  extinguished,  while  at  the  same  time  A  is  illumi- 
nated. The  Stentors  then  turn  and  move  toward  B.  They  may  be 
stopped  at  any  point  in  their  course  and  the  direction  of  swimming 
reversed  by  simultaneously  turning  off  one  light  and  turning  on  the 
other.  With  a  sensitive  culture  the  phenomena  take  place  with  con- 
siderable precision,  about  four-fifths  of  the  individuals  responding 
quickly  to  every  reversal  of  the  direction  from  which  the  light  comes. 

Under  these  circumstances  it  is  easy  to  observe  the  individuals  at  the 
moment  of  the  reversal  of  the  course.  The  observation  already  made 
is  confirmed  ;  the  animals  always  turn  at  the  moment  of  reversal  toward 
the  right  aboral  side.  The  reaction  is  thus  of  the  same  sort  that  occurs 
when  there  is  a  sudden  increase  in  illumination.  After  the  first  reaction 
the  anterior  end  is  pointed  in  a  new  direction.  If  this  new  direction 
is  away  from  the  source  of  light  the  animal  swims  forward  in  the 
course  so  laid  out.  If,  as  is  usually  the  case,  the  first  reaction  does 
not  result  in  directing  the  anterior  end  away  from  the  source  of  light, 
the  reaction  is  repeated,  and  this  may  occur  several  times.  Thus  the 
anterior  end  becomes  directed  successively  toward  every  quarter  ;  as 
soon  as  it  lies  toward  the  side  opposite  the  light  the  reaction  ceases. 
The  animal  now  swims  straight  ahead  (that  is,  in  a  spiral  with  a 
straight  axis)  away  from  the  source  of  light. 

Thus  while  it  is  clear  that  light  falling  from  one  side  produces  a 
well-defined  orientation,  this  orientation  does  not  take  place  in  such  a 
way  as  to  be  in  accordance  with  the  tropism  theory  as  set  forth,  for 
example,  by  Holt  &  Lee.  It  is  not  the  direct  action  of  the  light  on 
the  motor  organs  of  the  side  on  which  it  impinges  that  determines 
the  direction  of  turning,  but  the  latter  is  due  to  an  internal  factor. 
This  becomes  still  more  evident  when  the  conditions  are  so  arranged 
that  the  direction  of  turning  demanded  by  the  internal  factor  is  the 
opposite  of  that  required  by  the  tropism  theory. 

These  conditions  can  be  fulfilled  in  the  following  manner :  The 
light  to  be  turned  on  (Fig.  15)  is  so  moved  beforehand  that  its  rays 
shall  fall,  not  directly  on  the  anterior  end  of  the  Stentor,  but  obliquely 
at  an  angle  to  the  path  they  are  following.  The  animals  then  react 
as  before,  by  turning  toward  the  right  aboral  side.  It  often  happens 
that  this  involves  first  a  direct  turning  toward  the  light,  as  illustrated 
in  Fig.  16.  In  such  a  case  the  turning  is  continued  or  repeated  until 
the  anterior  end  is  directed  away  from  the  source  of  light.  We  have 
seen  the  same  result  produced  under  similar  conditions  in  the  experi- 
ments illustrated  in  Fig.  13. 

What  is  the  real  stimulus  to  the  production  of  the  motor  reaction 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


43 


which  results  in  orientation?  The  experiments  directed  precisely 
upon  this  point  show  that  the  stimulus  producing  the  motor  reaction 
is  an  increase  in  the  intensity  of  light  upon  the  sensitive  anterior  end. 
Now,  in  the  reaction  to  a  continuous  light  coming  from  one  side,  the 
conditions  are  present  for  exactly  such  changes  in  the  intensity  of  light 
at  the  anterior  end  as  would  induce  the  observed  reactions.  In  the 
spiral  course  the  animal  swerves  successively  in  many  directions.  In 
certain  directions  the  swerving  subjects  the  anterior  end  to  a  more 
intense  illumination.  This  change  acts  as  a  stimulus  to  produce  the 
motor  reaction,  which  carries  the  anterior  end  elsewhere.  In  other 
directions  the  swerving  leads  to  a  decrease  in  the  intensity  of  light 
affecting  the  anterior  end.  In  this  case  no  reaction  is  produced,  and  the 
organism  continues  to  swim  in  that  general  direction.  The  details  of 
this  method  of  reacting 
will  be  given  in  the  ac- 
count of  the  reactions  of 
Euglena,  where  the  mat- 
ter was  subjected  to  care- 
ful analytical  experimen- 
tation. The  evidence  all 
indicates  that  the  condi- 
tions in  Stentor  are  ex- 
actly parallel  to  those  in 
Euglena. 

We  may  sum  up  our 
results  on  Stentor  as  fol- 
lows :  A  change  from 

dark  to  light,  such  as  is  caused  by  swimming  from  a  shaded  into  an 
illuminated  region,  acts  as  a  stimulus  to  produce  a  typical  motor  reaction  ; 
the  Stentor  backs  and  turns  toward  the  right  aboral  side,  so  that  it 
returns  into  the  shaded  region.  A  change  in  the  illumination  of  the 
anterior  end  produces  the  same  effect  as  a  change  in  the  illumination 
of  the  entire  organism.  The  direction  from  which  the  light  comes  has 
no  observable  effect  on  this  reaction.  But  when  the  illumination  is 
uniform  and  the  light  comes  from  a  definite  direction,  then  light  fall- 
ing on  the  anterior  end  of  the  Stentor  causes  the  reaction,  while  light 
falling  upon  the  posterior  end  causes  none.  The  result  is  that  the 
animal  turns  (toward  the  right  aboral  side)  until  its  anterior  end  is 


Fig.  i6.* 


♦Fig.  i6. — Method  by  which  Stentor  becomes  oriented  to  light,  when  the  light 
falls  on  the  aboral  side  of  the  animal.  Stentor  turns,  as  shown  by  the  arrows, 
at  first  toward  the  light,  but  the  turning  is  repeated  or  continued  until  the 
anterior  end  is  directed  away  from  the  light 


44  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

directed  away  from  the  source  of  light,  and  swims  in  the  direction  so 
determined.  The  reaction  to  light  is  of  essentially  the  same  character 
as  the  reaction  to  other  usual  stimuli,  and  takes  place  by  what  we  may 
call  the  method  of  trial  and  error.  When  the  animal  comes  to  the 
boundary  of  a  lighted  area,  or  when  the  anterior  end  is  illuminated, 
this  constitutes  error  ;  the  animal  tries  some  other  direction,  and  repeats 
the  trial  till  the  condition  constituting  error  disappears. 

Are  these  results  in  agreement  with  all  the  observed  facts.?  The 
only  point  on  which  perhaps  question  might  arise  is  in  regard  to  the 
production  of  a  clearly  marked  orientation  such  as  we  find  shown  by 
Stentor  when   the   light  falls  upon  it  from  one  side.     In  this  case,  as 


Fig.  17.* 

we  have  seen,  Stentor  swims  directly  away  from  the  source  of  light, 
and  shows  thus  a  typical  orientation.  As  we  have  had  the  dictum 
that  a  motor  reaction,  such  as  I  have  described,  "  cannot  account  for 
an  orientation"  (Garrey,  1900,  p.  313),  it  will  be  well  to  examine  this 
matter  a  little  farther.  In  a  previous  paper  (Jennings,  1900,  a)  I  have 
shown  how  orientation  could  be  produced  through  a  motor  reaction  ; 
the  case  of  Stentor  exactly  realizes  the  possibility  there  set  forth.     If 


♦Fig.  17. — Diagram  to  illustrate  the  difference  between  the  method  of  orienta- 
tion tp  light  required  by  the  tropism  schema  and  that  which  actually  takes 
place.  To  light  coming  from  the  direction  shown  by  the  straight  arrows  the 
tropism  schema  requires  that  an  organism  in  the  position  x-y  should  attain  the 
position  y-z  by  turning  in  the  direction  indicated  by  the  (^broken)  arrow  a-i>. 
The  position  is  actually  attained  by  turning  in  the  direction  indicated  by  the 
long  arrow  c-d. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  45 

the  organism  is  at  first  not  oriented  to  lines  of  influence  coming  from  a 
certain  direction,  as  in  Fig.  17,  x-y^  and  then  becomes  oriented,  as  at 
Fig.  17,  y-z^  there  are  clearly  more  ways  than  one  by  which  the  orienta- 
tion can  be  produced.  The  essential  question  for  deciding  as  to  the 
nature  of  the  reaction  is  not  whether  orientation  occurs,  but  how  the 
orientation  is  brought  about.  This  consideration  has  been  too  often 
lost  sight  of  in  discussions  of  the  behavior  of  the  lower  organisms. 

According  to  the  theory  of  tropisms,  as  defined  by  Verworn,  Loeb, 
and  Holt  &  Lee,  the  orientation  should  be  brought  about  by  the  differ- 
ential action  of  the  external  agent  on  the  different  sides  of  the  organism  ; 
the  organism  should  turn  directly  into  the  line  of  action  of  the  external 
agent,  and  the  direction  of  turning  should  be  determined  by  an  external 
factor,  the  direction  of  the  infalling  rays,  or  the  side  on  which  they 
strike  the  organism.  Now  this  is  a  matter  which  can  be  settled  by 
direct  observation.  Direct  observation  shows  us  in  Stentor  that  orien- 
tation is  not  brought  about  in  the  manner  demanded  by  the  theory. 
The  direction  of  turning  is  determined  by  internal  fiictors.  The  reac- 
tion which  produces  orientation  is  identical  with  the  typical  reaction 
to  a  mechanical  shock,  to  chemicals,  to  heat  and  cold.  The  difference 
between  what  is  demanded  by  the  theory  of  tropisms  and  what  is 
actually  observed  may  be  made  quickly  evident  to  the  eye  by  Fig.  17. 
According  to  the  theory  of  tropisms  the  orientation  of  a  negatively 
phototactic  organism  should  take  place  by  turning  in  the  direction  of 
the  arrow  a-b\  in  a  Stentor  in  the  position  shown  {x-y')^  orientation 
actually  occurs  by  turning  in  the  opposite  direction,  as  shown  by  the 
arrow  c-d. 

The  further  question  then  arises  as  to  why  the  organism  remains 
oriented.  All  the  facts  point,  in  the  case  of  Stentor,  to  the  conclusion 
that  the  reaction  to  a  constant  light  is  due  to  the  intense  illumination 
on  the  sensitive  anterior  end.  As  soon,  therefore,  as  the  anterior  end  is 
turned  away  from  the  light,  as  is  the  case  in  the  position  y-z^  Fig.  17, 
there  is  no  further  cause  for  reaction ;  the  animal  therefore  remains 
with  its  anterior  end  directed  away  from  the  light ;  that  is,  it  remains 
oriented.  If,  as  a  result  of  reaction  to  some  other  stimulus,  or  in  any 
accidental  manner,  the  animal  comes  into  a  position  such  that  it  is  no 
longer  oriented,  the  '*  motor  reaction"  is  repeated  until  the  animal 
comes  again  into  the  position  of  orientation  in  which  it  is  no  longer 
stimulated. 

How  does  the  method  of  reaction  to  light  here  described  for  Stentor 
agree  with  what  we  know  of  light  reactions  in  other  ciliates.?  As 
noted  in  the  introductory  paragraphs,  comparatively  little  is  known  as 
to  light  reactions   in   this  group  of  organisms.     The  observations  of 


1    i     I    I 


46  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Engelmann  (1882,  a)  on  the  light  reactions  of  certain  green  ciliates 
(^Paramecium  bursaria^  Stentor  viridis^  etc.)  were  made  before  the 
typical  motor  reaction — the  turning  toward  a  certain  structurally  de- 
fined side— had  been  observed  in  any  of  the  infusoria.  Engelmann, 
therefore,  paid  no  attention  to  this  point.  Yet  there  is  much  in  his 
account  of  the  reactions  to  light  in  these  organisms  to  suggest  that 
it  takes  place  in  a  way  similar  to  that  which  I  have  described  above 
for  Stentor  cceruleus.  Indeed,  Engelmann's  account,  so  far  as  it 
goes,  fits  precisely  into  the  reaction  method  which  I  have  described 
above.  He  found,  as  I  have,  that  the  organisms  react  either  when  only 
the  anterior  end  is  aflfected,  or  when  the  entire  organism  is  flooded  with 
light  from  beneath.  The  reaction  consists  in  a  sudden  turn  to  one  side, 
or  a  sudden  start  backward,  just  as  in  Stentor  cceruleus.  The  only 
point  which  is  lacking  in  Engelmann's  account  is  the  observation  as 

to  which  side  the  organism 
turned  ;  to  this  point  he  did 
not  direct  his  attention. 

It  is  interesting  to  note  that 
in  the  account  given  by  Ver- 
worn  (1889,  Nachschrift)  of 
the  reaction  to  light  in  Pleu- 
ronema  chrysalis  there  is 
p,       T,„  ""     nothing  tending  to  support 

the  theory  of  an  orienting  tro- 
pism.  According  to  Verworn  the  reaction  of  Pleuronema  to  light  is  by 
a  sudden  leap  ("  Sprungbewegung"),  which  is  repeated  several  times  if 
the  light  continues.  This  sudden  leap  seems  identical  with  the  *'  motor 
reflex"  which  I  have  described  as  the  typical  reaction  to  stimuli  in 
many  ciliates,  and  which  consists  usually  in  a  leap  backward,  followed 
by  a  turning  toward  a  structurally  defined  side.  It  is  in  this  manner, 
as  we  have  seen,  that  Stentor  cceruleus  reacts  to  light  and  the  reac- 
tion, as  in  Pleuronema,  is  often  repeated  many  times. 

Thus  the  other  carefully  studied  accounts  of  reaction  to  light  in  the 
Ciliata,  while  incomplete,  agree  so  far  as  they  go  with  that  which  I 
have  given  for  Stentor,  and  contain  nothing  to  suggest  the  idea  of  an 
orienting  tropism  dependent  upon  unequal  stimulation  of  the  motor 
organs  on  the  opposite  sides  of  the  animal. 


♦Fig.  18. — Diagram  of  the  reaction  of  Stentor  to  Hght,  after  Holt  &  Lee. 
Stentors  are  confined  in  a  vessel  behind  a  wedge-shaped  prism  containing  a 
substance  which  partly  cuts  off  the  light,  so  that  one  end  of  the  vessel  is  darker 
than  the  other.  The  usual  course  of  a  Stentor  near  the  lighter  end  is  shown  by 
the  broken  line. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


47 


Davenport's  reference  (Davenport,  1897,  p.  189)  to  the  negative 
light  reaction  of  Stentor  makes  no  attempt  to  explain  the  mechanism  of 
the  reaction.  Holt  &  Lee  (1901)  have  given  an  account  of  some  fea- 
tures of  the  light  reaction  of  Stentor  cceruleus.  They  did  not  attempt 
to  determine  directly  the  mechanism  of  the  reactions,  by  observation 
of  the  exact  movements  of  the  organism.  Specifically,  they  made  no 
observations  to  determine  w^hether  Stentor  becomes  oriented  by  turn- 
ing directly  aw^ay  from  the  source  of  light  or  only  indirectly  through 
a  "  motor  reaction  "  such  as  I  have  described.  They  did  attempt,  how- 
ever, to  show  that  the  gross  phenomena  observed  might  be  interpreted 
in  accordance  with  the  prevailing  theory  of  tropisms  set  forth  on  page 
7  of  the  present  volume.  It  will  be 
well,  therefore,  to  examine  their  obser- 
vations in  order  to  determine  whether 
they  contain  anything  inconsistent  with 
the  account  set  forth  in  the  present 
paper. 

Holt  &  Lee  studied  the  behavior  of 
Stentor  in  an  elongated  trough  which 
was  lighted  from  one  side.  The  light 
passed  through  a  prism  which  con- 
tained a  translucent  fluid  (a  weak  solu- 
tion of  India  ink),  by  means  of  which 
a  portion  of  the  light  was  cut  out  (Figs. 
18  and  19). 

At  the  thicker  end  of  the  prism  more 
light  was  cut  out,  hence  this  end  of  the 
trough  (Fig.  19,  D)  was  darker  than 
the  opposite  end  (Z).  It  was  found 
that  when  Stentors  were  placed  in  the  trough  close  behind  the  prism 
(ato,  Fig.  19)  they  turned  and  swam  away  from  the  lighted  side  till  the 
back  of  the  trough  was  reached  {a  to  </,  Fig.  19) .  This  is  of  course  ex- 
actly what  happens  when  no  prism  is  interposed.  Reaching  the  back  of 
the  trough  the  animals  give  the  motor  reaction  (by  backing,  then  turning 
toward  the  right  aboral  side),  thus  coming  into  either  the  position  e  or  the 
positiony  (Fig.  19).     They  then  swim  forward  again,  strike  the  wall, 


Fig.  19. 


*  Fig.  19.— Reaction  of  such  an  infusorian  as  Stentor  to  light,  under  the  con- 
ditions shown  in  Fig.  18.  After  Holt  &  Lee.  The  animal  in  the  position  *-y, 
close  behind  the  prism,  turns  and  swims  to  the  position  </,  where  it  comes  against 
the  rear  wall  of  the  trough.  It  then  turns  either  into  the  position  e,  toward  the 
darker  end  Z>,  or  into  the  position/,  toward  the  lighter  end  L.  In  the  latter  case 
it  usually  soon  reacts  again,  and  by  repetition  of  the  reaction  it  finally,  as  a  rule, 
becomes  directed  toward  D.  Thus,  finally,  most  of  the  Stentors  collect  in  the 
dark  end  of  the  trough. 


4$  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

and  repeat  the  reaction.  This  is  repeated  many  times  until  the  organ- 
isms are  swimming  either  toward  the  end  D  or  toward  the  end  L.  In 
course  of  time  it  is  found  that  the  preponderance  of  movement  is  toward 
the  dark  end  Z>,  so  that  the  majority  of  the  Stentors  are  gathered  at  D. 
Why  this  should  be  so  is  explained  by  Holt  &  Lee  as  follows : 

The  reason  why  the  Stentors  went  eventually  in  greater  numbers  toward  D, 
and  thus  appeared  oftener  to  choose  e  than  /",  is  that  such  Stentors  as  went  to  e 
progressed  farther  toward  D  than  those  which  went  to/"  could  progress  toward 
L,.  These  latter  would  soon  strike  the  wall  a  second  time,  now  pretty  nearly  at 
right  angles,  and  during  the  recoil  the  light  stimuli  would  favor  a  return  to  d. 
It  appears  then  amplj'  possible  that  the  circumstance  that  the  organism  encoun- 
ters the  wall  of  the  trough  at  an  acute  angle  is  sufficient  to  cause  its  farther 
progress  to  be,  in  the  long  run,  toward  D. 

There  is  evidently  nothing  in  this  account  which  is  inconsistent  with 
the  method  of  light  reaction  which  I  have  described.  On  the  contrary, 
the  reason  why  the  organisms  finally  swim  toward  the  dark  end  and 
gather  there  becomes  much  more  evident  when  the  reaction  method 
that  I  have  described  is  taken  into  consideration.  Let  us  suppose  that 
the  Stentors,  after  striking  the  back  of  the  trough,  turn  in  equal  numbers 
toward  D  and  toward  Z.  In  those  swimming  toward  D  the  anterior 
end  is  directed  away  from  the  source  of  strongest  light  (due  to  reflection 
from  the  lighted  end  of  the  dish  /,),  and  the  animals  are  passing  into  a 
region  of  less  intense  light.  There  is  thus  nothing  to  cause  the  "  motor 
reaction,"  with  its  accompanying  change  in  the  direction  of  movement. 
In  the  Stentors  swimming  toward  Z,  on  the  other  hand,  the  strongest 
light  falls  on  the  anterior  end,  and  the  organisms  are  passing  into  a 
region  of  more  intense  light.  Either  of  these  factors  taken  separately 
may,  as  we  have  seen,  cause  the  motor  reaction  (the  turning  toward 
the  right  aboral  side),  thus  changing  the  direction  in  which  the  Stentors 
swim.  The  animals  which  start  to  swim  toward  L  will  therefore  soon 
be  turned,  and  only  when  the  direction  of  movement  is  toward  D  will 
there  be  no  cause  for  further  change. 

The  observations  of  Holt  &  Lee  are  thus  quite  in  harmony  with 
the  reaction  method  which  I  have  described,  and  indeed  receive 
illumination  when  this  reaction  method  is  taken  into  consideration. 

In  the  "  fourth  case"  discussed  by  Holt  &  Lee  {loc.  cit.^  pp.  475" 
478),  the  two  factors  mentioned  as  determining  the  turning  of  the 
Stentors  away  from  the  end  L  would  work  in  opposite  directions  ;  only 
experience  can  tell  which  would  be  more  eflective.  As  Holt  &  Lee 
do  not  state  specially  that  they  observed  the  reactions  of  Stentor  under 
these  conditions  no  comment  is  required.  Experiments  of  this  character 
will  be  further  considered  after  we  have  described  reactions  to  light 
in  flagellates. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


49 


THE  FLAGELLATA. 


In  the  following  pages  we  shall  examine  the  method  of  reaction  to 
light  in  the  flagellates  Euglena  viridis^  Cryptomonas  i 

ovata^  and  a  species  of  Chlamydomonas. 

EUGLENA  VIRIDIS. 

Euglena  viridis  swims  in  a  spiral  path,  continu- 
ally swerving  toward  that  side  which  bears  the  larger 
''  lip  "  and  the  eye,  the  so-called  dorsal  side  (Fig.  20). 
Its  motor  reaction  to  most  stimuli  is  by  a  sudden  pro- 
nounced turning  toward  the  dorsal  side ;  that  is,  by 
swerving  still  farther  toward  the  same  side  toward 
which  it  swerves  in  its  normal  swimming.  Thus  the 
direction  of  its  path  is  changed  (Jennings,  1900). 

The  general  features  of  the  reaction  of  Euglena  to 
light  have  been  well  worked  out  by  Englemann 
(1882,  a)  and  Wager  (1900).  These  authors  show 
that  Euglena  collects  in  lighted  regions.  The  organ- 
isms pass  into  a  lighted  area  without  reaction.  But 
on  coming  to  the  outer  boundary  of  such  an  area, 
where  they  would  pass  out  into  the  dark,  they  react 
by  turning  round  and  passing  back  into  the  light. 
The  collections  of  Euglenae  in  lighted  areas  are  thus 
brought  about  in  much  the  same  manner  as  the  col- 
lections of  Paramecia  in  regions  containing  a  weak 
acid  (Jennings,  1899).  If  diffuse  light  falls  from  one 
side  on  water  containing  Euglenas,  the  organisms  swim 
toward  the  source  of  light.  But  if  strong  sunlight 
falls  upon  them  they  swim  away  from  the  source  of 
light. 

Engelmann  showed  that  the  colorless  anterior  end 
is  the  part  that  is  chiefly  sensitive  to  variations  of  light. 
Often  the  organism  in  a  lighted  area,  on  reaching  the 
edge,  reacts  by  turning  when  only  the  colorless  tip 
has  passed  into  the  darkness. 

The  precise  method  of  reaction  to  light,  the  direc- 
tion of  turning  in  becoming  oriented  or  in  passing 
back  into  the  lighted  area,  was  not  worked  out  by  the  authors  named. 
To  this  point  we  shall  direct  our  attention. 

When  a  large  number  of  Euglenae  are  swimming  toward  the  source 
of  light,  if  the  illumination  is  suddenly  decreased  in  anyway,  they  give 


Fig.  20* 


♦  Fig.  20  shows  the  spiral  path  of  Euglena  in  its  ordinary  swimming. 


50  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

the  typical  motor  reaction  described  in  my  previous  paper  as  a  response 
to  other  classes  of  stimuli  (Jennings,  1900,  p.  235).  That  is,  they 
turn  at  once  toward  the  dorsal  side  (that  bearing  the  larger  lip  and  the 
eye).  This  is  very  easily  seen  when  the  Euglenae  are  mounted  in  the 
ordinary  manner  in  a  thin  layer  of  water  on  a  glass  slide  and  observed 
with  the  microscope  in  the  neighborhood  of  a  window.  If  the  hand 
is  interposed  between  the  slide  and  the  window  all  the  Euglenae  react 
in  the  way  just  described. 

The  reaction  is  a  very  sharp  and  striking  one  and  produces  a  very 
peculiar  impression.  At  first  all  the  Euglenae  are  swimming  in  parallel 
lines  toward  the  window.  As  soon  as  the  shadow  of  the  hand  falls  on 
the  slide  the  regularity  is  destroyed  ;  every  Euglena  turns  strongly  and 
may  seem  to  oscillate  from  side  to  side  in  the  manner  described  later. 

The  turning  is  often  preceded  by  a  slight  movement  backward. 
This  was  not  observed  in  the  reactions  to  other  stimuli  (Jennings,  1900, 
p.  235),  though  it  agrees  with  what  we  find  in  most  other  ciliates  and 
flagellates.  In  Euglena  the  reaction  to  variations  in  the  intensity  of 
light  seems  more  sharply  defined  than  to  most  other  stimuli.  The  fact 
that  the  turning  is  always  toward  the  dorsal  side  is  observable  with  the 
greatest  ease.  It  is  particularly  evident  when  the  organisms  are  con- 
fined to  a  thin  layer  of  water,  so  that  they  cannot  swerve  up  or  down, 
but  only  to  the  right  or  left. 

The  reaction  occurs  whenever  the  light  is  suddenly  decreased  in  any 
way.  Certain  different  conditions  under  which  it  occurs  deserve  special 
mention,  (i)  As  we  have  seen,  the  reaction  occurs  when  a  screen  is 
brought  between  the  organisms  and  the  source  of  light  toward  which 
they  are  swimming.  (2)  It  also  occurs  when  the  illumination  is  de- 
creased by  cutting  off  light  from  some  other  source  than  that  toward 
which  they  are  swimming.  Thus  the  organisms  on  the  stage  of  the 
microscope  may  be  lighted  from  below,  by  the  substage  mirror,  and  at 
the  same  time  may  receive  light  from  the  window  at  one  side  of  the 
preparation.  They  swim  toward  the  window,  since  the  light  from  that 
quarter  is  much  stronger  than  that  from  below.  If  now  the  light  from 
below  is  suddenly  decreased  by  closing  the  iris  diaphragm,  the  Euglenae 
react  as  usual  by  turning  strongly.  This  is  notwithstanding  the  fact 
that  the  proportion  of  light  coming  from  the  window,  to  which  they 
were  oriented,  is  now  greater  than  before,  so  that  it  might  be  supposed 
that  they  would  remain  more  strongly  oriented  than  ever.  For  the  rest, 
the  disturbed  orientation  is  soon  restored.  (3)  The  reaction  occurs 
when  the  decrease  in  illumination  is  due  to  the  movements  of  the 
Euglenae  ;  that  is,  when  the  swimming  organisms  come  to  the  edge  of 
a  lighted  region  where  they  would,  if  the  course  were  continued,  pass 
into  the  darkness.     As  a  result  of  the  reaction  they  return  into  the  light. 


REACTIONS    TO    LIGHT    IN    CII.IATES    AND    FLAGELLATES.  5 1 

The  reaction  occurs  at  a  decrease  in  illumination  not  only  when  the 
organisms  are  oriented  and  swimming  toward  the  source  of  light,  but 
also  when  they  are  not  oriented  and  are  merely  scattered  in  a  weakly 
lighted  area.  Further,  in  cases  where  most  of  the  Euglense  are  oriented 
and  swimming  toward  a  source  of  light,  a  number  of  specimens  will 
always  be  found  that  are  not  oriented  at  all,  or  are  swimming  away 
from  the  source  of  light.  Such  individuals  react  to  a  sudden  decrease 
in  illumination  in  the  same  manner  as  do  the  specimens  that  are  oriented 
with  the  anterior  end  toward  the  source  of  light.  This  result  may  be 
observed  in  a  curious  way  as  a  consequence  of  the  fact  that  it  requires 
some  time  for  the  light  to  produce  its  orienting  effect.  Thus,  if  the 
Euglenae  are  placed  between  a  weak  and  a  strong  light  they  swim  toward 
the  strong  light.  If,  now,  the  strong  light  is  cut  off,  they  react  in  the 
usual  way  and  swim  toward  the  weak  light.  Now  the  strong  light 
may  be  restored  ;  the  Euglenae  continue  for  a  few  seconds  to  swim  toward 
the  weak  light,  thus  away  from  the  strong  light.  If  while  they  are 
swimming  in  this  manner  the  strong  light  is  cutoff,  the  Euglenae,  swim- 
ming away  from  it,  react  in  the  usual  manner,  by  turning  strongly 
toward  the  dorsal  side. 

The  usual  reaction  may  be  produced  by  a  decrease  in  illumination 
that  is  not  sufficient  to  cause  a  permanent  change  in  orientation.  Thus 
the  Euglenae  on  a  slide  or  in  a  shallow  dish  may  be  lighted  from  a 
window  at  one  side.  By  passing  a  small  screen  in  front  of  the  window 
at  some  distance  from  the  preparation  a  portion  of  the  light  is  cut  off; 
the  Euglenae  then  respond  in  the  usual  way,  by  swerving  toward  the 
dorsal  side.  The  movement  thus  becomes  very  irregular.  Since  the 
Euglenae  continue  to  revolve  on  their  long  axes  the  dorsal  side  may  lie 
first  to  the  (observer's)  right,  then  to  the  left.  The  Euglenae  all  seem, 
therefore,  to  vibrate  from  side  to  side.  This  is  the  *' Erschiitterung  " 
or  trembling  described  by  Strasburger  (187S)  as  occurring  in  swarm- 
spores  when  the  illumination  is  changed ;  it  will  be  understood  better 
when  we  have  considered  more  in  detail  the  mechanism  of  the  reactions. 
Meanwhile  the  screen  retains  its  position,  but  still  admits  more  light 
from  the  direction  of  the  window  than  from  any  other  direction.  The 
reaction  of  the  Euglenae,  therefore,  soon  ceases ;  their  orientation  is 
restored  in  the  way  to  be  described  later,  and  they  continue  to  swim 
toward  the  window. 

This  experiment  is  an  important  one.  It  shows  that  the  typical  reac- 
tion may  be  produced  by  a  decrease  in  light  that  is  not  sufficient  to 
permanently  destroy  the  orientation.  Thus  it  is  clearly  the  decrease 
in  illumination  to  which  the  organisms  react ;  not  to  a  change  in  the 
direction  of  the  light  rays.  The  experiment  shows  further  that  it  is 
not  the  absolute   amount  of  light  that  determines  the  reaction.     Some 


53  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

time  after  the  decrease  in  illumination  takes  place  the  organisms  behave 
just  as  they  did  before,  swimming  in  the  same  direction.  Further, 
the  illumination  may  be  decreased  very  slowly  to  the  same  extent 
without  causing  a  reaction.  If  the  screen  is  at  first  far  away  from  the 
preparation  and  is  then  slowly  moved  to  the  position  it  occupied  in 
the  experiment  just  described  no  reaction  is  produced.  It  is  only  the 
sudden  change  that  has  caused  the  reaction.  The  change,  however, 
need  not  be  a  very  marked  one  in  order  to  be  effective. 

Our  experiments  thus  far  have  shown  that  in  a  moderate  light  Eu- 
glena  reacts  to  a  decrease  in  illumination.  But  the  absolute  amount  of 
light  present  has  an  effect  on  the  reaction.  If  the  light  is  very  strongly 
increased  the  same  reaction  is  produced  as  when  the  light  is  decreased. 
If  while  the  organisms  are  swimming  toward  a  moderately  lighted 
window  direct  sunlight  is  allowed  to  fall  upon  them,  they  respond  in 
the  same  way  as  to  a  sudden  decrease  in  illumination  ;  that  is,  they 
turn  strongly  toward  the  dorsal  side,  continuing  or  repeating  the  re- 
action till  the  anterior  end  is  directed  away  from  the  source  of  light. 
They  now  continue  to  swim  in  that  direction,  the  positive  reaction 
having  been  transformed  into  a  negative  one.  Thus  under  intense 
light  the  conditions  of  stimulation  are  the  opposite  of  those  under 
moderate  light.  This  is  paralleled  in  the  reactions  of  the  infusoria  to 
chemicals  ;  often  a  strong  solution  of  a  certain  chemical  produces  a  re- 
action under  opposite  conditions  from  those  in  which  a  weak  solution 
of  the  same  chemical  is  effective. 

Let  us  now  proceed  to  a  more  careful  study  of  the  reaction  itself. 
The  reaction  which  occurs  when  the  illumination  is  changed  is  really 
an  accentuation  of  a  certain  feature  of  the  usual  movements.  Euglena, 
as  we  know,  revolves  on  its  long  axis  as  it  swims  forward,  and  at  the 
same  time  it  swerves  toward  the  dorsal  side.  The  resulting  path  is 
therefore  a  spiral  one  (Fig.  20).  The  usual  reaction  to  a  stimulus  is 
an  accentuation  of  this  normal  swerving  toward  the  dorsal  side,  as  com- 
pared with  the  other  factors  in  the  swimming;  the  organism  suddenly 
swerves  so  much  farther  than  usual  in  this  direction  that  the  path  may 
be  completely  changed.  If  the  reaction  is  a  very  decided  one  the  revo- 
lution on  the  long  axis  and  the  movement  forward  may  cease  during 
the  swerving  toward  the  dorsal  side ;  the  anterior  end  then  describes 
the  arc  of  a  circle  about  the  posterior  end  as  a  center.  In  a  less  pro- 
nounced reaction  the  revolution  on  the  long  axis  continues.  The  circle, 
described  by  the  anterior  end  is  then  less  and  the  whole  body  describes 
the  surface  of  a  cone,  or  a  frustum  of  a  cone,  as  illustrated  in  Fig.  21. 
Every  gradation  exists  between  the  normal  spiral  course  and  the  strong 
reaction  in  which  the  anterior  end  swings  in  a  circle  about  the 
posterior  end  as  a  center. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


53 


When  oriented  and  swimming  toward  the  source  of  light  the  swerv- 
ing toward  the  dorsal  side  is  comparatively  slight.  As  seen  from 
above,  the  organisms  seem  merely  to  oscillate  a  very  little  from  side  to 
side  as  they  revolve  on  the  long  axis.  Careful  examination  shows  that 
the  swerving  is  always  toward  the  dorsal  side,  as  in  Fig.  20,  the  alter- 
nations in  direction  being  due  to  the  alternations  of  position  of  the 
dorsal  side.  Now,  when  the  illumination  is  suddenly  decreased,  the 
Euglenas  at  once  swing  much  farther  than  usual  toward  the  side  to 


Fig.  21.* 

which  they  are  already  swerving,  that  is,  toward  the  dorsal  side.  If 
the  decrease  in  illumination  is  not  very  great,  so  that  the  stimulus  is 
not  a  strong  one,  the  swerving  is  not  very  great,  and  the  organism  at 
the  same  time  continues  to  revolve  on  its  long  axis  ;  thus  the  anterior 
end  describes  a  circle  and  the  whole  body  describes  the  surface  of  a 


*FiG.  21. — Diagram  to  illustrate  reaction  of  Euglena  when  the  illumination 
is  decreased.  The  Euglena  is  swimming  forward  at  i ;  when  it  reaches  the 
position  2  the  illumination  is  decreased.  Thereupon  the  organism  swerves 
strongly  toward  the  dorsal  side.  This  swerving,  combined  with  the  revolution 
on  the  long  axis,  causes  the  anterior  end  to  swing  about  a  circle,  so  that  the 
Euglena  occupies  successively  the  positions  2,  3,  4,  5.  6,  etc.  From  any  of  these 
positions  it  may  start  forward,  as  indicated  by  the  arrows,  if  the  condition 
causing  the  reaction  ceases  to  act.  In  the  figure  the  Euglena  is  represented  as 
swimming  forward  from  the  position  6. 


54 


THE    feKHAVIOR    OF    LOWER    ORGANISMS. 


cone,  or  the  frustum  of  a  cone,  as  indicated  in  Fig.  21.  The  result,  as 
seen  from  above,  is  that  all  the  specimens  seem  to  vibrate  from  side  to 
side  ;  in  other  words,  they  are  taken  with  a  sudden  oscillation  or  trem- 
bling. This  oscillation  when  the  intensity  of  the  light  is  suddenly 
changed  was  observed  by  Strasburger  (1878, 
pp.  25  and  50)  in  flagellate  swarm-spores ;  he 
speaks  of  it  as  *' Erschiitterung "  or  "  Zit- 
tern."  During  this  oscillation  the  anterior  end 
becomes  pointed  successively  in  many  different 
directions,  as  Fig.  21  show^s.  When,  now,  the 
usual  forward  course  is  resumed  (with  only  the 
usual  amount  of  swerving  toward  the  dorsal 
side),  the  animal  follows  one  of  these  directions. 
Thus  its  path  is  changed  (Fig.  22).  Strasburger 
(1878,  p.  25)  noticed  that  the  path  followed  after 
the  oscillation  was  oblique  to  the  former  path. 
As  a  study  of  Figs.  21  and  22  will  show,  this  is  a 
necessary  consequence  of  the  increased  swerving 
toward  the  dorsal  side,  to  which  the  oscillation 
itself  is  due.  All  these  relations  become  much 
clearer  if  a  model  of  an  actual  spiral  is  studied  ; 
it  is  difficult  to  represent  them  upon  a  plane 
surface. 

If  the  stimulus  is  stronger,  as  when  there  is  a 
greater  decrease  in  illumination,  the  swerving 
toward  the  dorsal  side  is  much  greater ;  the  or- 
ganism wheels  far  to  that  side,  so  that  the  spiral 
course  seems  entirely  interrupted.  But  there  is 
really  nothing  in  this  reaction  differing  in  prin- 
ciple from  what  is  happening  in  the  normal 
forward  swimming.    If  the  swerving  toward  the 

f  dorsal  side  is  long  continued  the  specimen  may 

be  seen  to  swing  first  far  to  the  (observer's)  right, 

^  ^  then,  after  it  has  revolved  on  the  long:  axis,  far 

Fig.  22.*  ^  ' 

to  the  (observer's)  left;  in  reality  it  swings  an 

equal  amount  upward  and  downward  and  in  intermediate  directions. 

It  may,  however,  swing  at  once  so  far  to  the  dorsal  side  that  the  new 


*  Fig.  22. — Shows  the  spiral  path  of  Euglena,  illustrating  the  eifect  of  a 
slightly  marked  reaction.  At  a  the  illumination  is  decreased;  the  organism 
therefore  swerves  toward  the  dorsal  side,  causing  the  spiral  to  become  wider. 
At  b  the  ordinary  method  of  swimming  is  resumed;  since  at  this  point  the 
organism  was  more  inclined  to  the  axis  of  the  spiral  than  before  the  reaction, 
the  new  course  lies  at  an  angle  with  the  previous  one.     Compare  with  Fig.  21. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


55 


course  forms  a  right  angle,  or  a  still  greater  angle,  with  the  original 
course  ;  if  the  turning  is  through  iSo°,  the  course  will  be  squarely 
reversed.  Indeed,  sometimes  the  organism  swings  around  an  entire 
circle  or  more.  When  the  usual  method  of  swimming  is  resumed  after 
such  reactions  as  those  just  described,  the  course  has  been  completely 
changed. 

Strasburger  (1S78,  p.  25)  noticed  that  after  a  decrease  in  illumina- 
tion flagellate  swarm-spores  often  turn  strongly  to  one  side  or  even 
describe  circles.  But  he  did  not  notice  that  the  turning  was  always 
toward  the  same  side  of  the  organism,*  and  did  not  perceive  the  relation 
between  this  effect  and  the  remainder  of  the  reaction. 


Fig.  23. t 

This  method  of  reaction  is  particularly  striking  when  the  Euglenae 
are  confined  to  a  very  thin  layer  of  water  between  the  slide  and  the 
cover  glass,  so  that  they  cannot  swerve  up  or  down.  When  the  light 
is  decreased,  we  will  suppose  that  the  dorsal  side  is  to  the  (observer's) 
left.     The  Euglena  then  swings  far  to  the  left.     At  the  same  time  it 


♦Naegeli  (i86o,  p.  96)  had,  however,  before  Strasburger,  observed  that  in  such 
swarm-spores  the  same  side  always  faces  the  outside  of  the  spiral  path.  This 
observation,  which  really  contained  the  germ  of  a  correct  understanding  of  the 
reactions  to  stimuli,  seems  hardly  to  have  been  noticed  by  later  writers, 

t  Fig.  23. — Diagram  of  the  method  by  which  Euglena  becomes  oriented  with 
anterior  end  toward  the  source  of  light.  At  i  the  Euglena  is  swimming  toward 
the  source  of  light.  When  it  reaches  the  position  2  the  light  is  changed  so  as 
to  come  in  the  direction  indicated  by  the  arrows  at  the  right.  As  a  consequence 
of  tlie  decrease  in  illumination  of  the  anterior  end  thus  caused,  the  orijanism 


56  THK    BEHAVIOR    OF    LOWER    ORGANISMS. 

revolves  on  its  long  axis,  bringing  the  dorsal  side  down.  Since  it  can 
not  swing  downward,  owing  to  the  narrow  space,  this  has  little  effect 
on  the  reaction,  save  to  stop  the  movement  to  tlie  left.  Now,  by  con- 
tinued rotation  the  dorsal  side  has  come  to  lie  to  the  (observer's) 
right ;  the  Euglena  may  then  be  seen  to  swing  far  to  the  right.  In  each 
case  under  these  conditions  it  is  at  once  evident  by  observing  the 
larger  lip  at  the  anterior  end  that  tiie  organism  is  swinging  toward 
the  dorsal  side. 

This  method  of  reaction  is  very  effective  in  preventing  Euglena  from 
passing  from  an  illuminated  region  to  a  shaded  one.  As  soon  as  the 
anterior  end  enters  the  shadow,  the  animal  swings  far  toward  the  dor- 
sal side  till  the  anterior  end  is  brought  again  into  the  light,  repeating 
the  reaction  if  necessary.  There  is  then  no  further  cause  for  reaction. 
The  reaction  to  a  very  strong  increase  of  illumination  is,  as  we  have 
seen,  identical  with  that  to  a  decrease  in  illumination. 

In  our  experiments  thus  far  we  have  directed  attention  primarily  to 
the  effects  of  changes  in  the  intensity  of  illumination,  and  have  found 
that  such  changes  produce  a  motor  reaction  independently  of  the  direc- 
tion of  the  light  rays.  But  it  is  of  course  well  known  that  Euglena 
does  react  with  reference  to  the  direction  of  the  light  rays.  Euglenae 
swim  toward  the  source  of  light  when  weakly  illuminated,  away  from 
the  source  of  light  when  strongly  illuminated.  If  Euglenae  are  swim- 
ming at  random  in  a  diffuse  light  they  soon  become  oriented  when  the 
light  is  allowed  to  act  on  them  from  one  side,  even  if  the  intensity  of 
illumination  remains  the  same.  Or,  if  Euglenae  are  swimming  toward 
a  source  of  very  weak  light  and  a  stronger  light  is  allowed  to  act  upon 
them  from  the  opposite  side,  they  become  oriented,  in  time,  with 
anterior  ends  toward  the  stronger  light.  In  examining  this  dependence 
of  the  direction  of  swimming  on  the  direction  of  the  rays  of  light,  we 


swerves  strongly  toward  the  dorsal  side,  at  the  same  time  continuing  to  revolve 
on  the  long  axis.  It  thus  occupies  successively  the  positions  2,  3,  4,  5,  6.  In 
passing  from  3  to  6  the  illumination  of  the  anterior  end  is  increased;  hence  the 
reaction  nearly  or  quite  ceases.  In  the  next  phase  of  the  spiral,  therefore,  the 
organism  swerves  but  a  little  toward  the  dorsal  side — from  7  to  8.  But  this 
movement  causes  a  decrease  in  the  illumination  of  the  anterior  end,  and  this 
change  induces  again  the  strong  swerving  toward  the  dorsal  side.  Hence  in 
the  next  phase  of  the  spiral  the  organism  swings  through  9  and  10  to  11.  In 
this  movement  again  the  illumination  of  the  anterior  end  is  increased;  hence 
the  reaction  ceases,  so  that  from  12  the  organism  swerves  only  as  far  as  13. 
Then  owing  to  the  decrease  in  illumination  caused  by  this  movement,  the 
swerving  increases,  so  that  the  Euglena  swings  from  13  through  14  and  15  to  16. 
Now  it  is  directed  toward  the  source  of  light,  and  such  swerving  as  takes  place 
in  the  spiral  course  neither  increases  nor  decreases  the  illumination  of  the 
anterior  end.  Hence  there  is  no  further  reaction;  the  Euglena  continues  to 
swim  forward  in  the  direction  16-17. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES. 


SI 


shall  have  to  keep  in  mind  two  questions :  First,  how  is  the  position 
of  orientation  brought  about?  Second,  what  is  the  real  stimulus  in 
producing  orientation? 

To  answer  the  first  question  we  must  observe  the  movements  of  the 


■^^^^ 


-^- 


)a 


^ 


\h 


V 


Fig.  24.* 

organism  at  the  time  orientation  occurs.  Observation  of  the  individ- 
uals as  they  are  becoming  oriented  shows  that  orientation  is  brought 
about  through  the  same  motor  reaction  that  we  have  already  described  ; 


*  Fig    24. — Path   followed   by  Euglena    when  the  direction    of    the   light    is 
changed.     From  i  to  2  the  organism  swims  forward  in  the  usual  spiral  path 
At  2  the  position  of  the  source  of  light  is  changed,  so  that  it  now  comes  from 
behind.     The  organism  then  begins  to  swerve  farther  than  usual  toward  the 


58  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

that  is,  by  a  turning  toward  the  dorsal  side.  The  simplest  case  is  per- 
haps that  of  the  reversal  of  orientation,  produced  when  strong  sunlight 
is  allowed  to  fall  from  in  front  upon  specimens  that  are  swimming 
toward  a  diffusely  lighted  window.  Under  these  circumstances,  as 
we  have  seen,  the  Euglenae  turn  toward  the  dorsal  side,  changing  their 
course.  They  may  turn  directly  through  180°,  in  which  case  they  are 
at  once  oriented  with  anterior  ends  away  from  the  light ;  but  usually 
the  orientation  is  less  direct  than  this.  The  reaction  is  generally 
repeated  several  times.  Through  its  continued  swerving  toward  the 
dorsal  side,  combined  with  the  revolution  on  the  long  axis,  the  organism 
directs  its  anterior  end  successively  in  every  direction.  When  the 
anterior  end  has  finally  come  into  a  position  where  it  points  away  from 
the  strong  light  the  reaction  ceases,  and  the  organism  swims  forward 
in  the  usual  way.  The  details  of  the  orienting  reaction  will  be  brought 
out  more  fully  in  the  following  account  of  the  way  in  which  the  anterior 
end  becomes  directed  toward  a  source  of  light  of  moderate  intensity. 
Let  us  now  take  a  case  in  which  the  change  in  the  direction  of  the 
rays  of  light  is  not  accompanied  by  a  change  in  the  intensity  of  illumi- 
nation. Euglense  are  swimming  about  at  random  in  a  diffuse  light 
when  all  the  light  is  allowed  to  fall  upon  them  from  one  side.  They 
then  become  oriented,  with  anterior  ends  directed  toward  the  source  of 
light.  Or,  the  organisms  are  swimming  toward  a  source  of  light  when 
the  direction  of  the  light  rays  is  changed  or  reversed  by  quickly 
moving  the  source  from  which  the  light  comes.  The  Euglenae  then 
after  a  time  become  reoriented.  Under  such  circumstances  there  is  no 
sudden,  decided  reaction,  such  as  occurs  when  the  illumination  is 
suddenly  decreased.  The  organism  merely  begins  to  swerve  farther 
toward  the  dorsal  side  than  usual.  Thus  the  spiral  has  become  wider, 
and  the  anterior  end  comes  to  be  pointed  successively  in  many  dif- 
ferent directions,  as  illustrated  at  1-6  in  Fig.  23.  In  some  of  these 
positions  the  anterior  end  is  directed  farther  away  from  the  source 
of  light,  as  at  3  ;  in  other  positions  more  nearly  toward  the  source 
of  light,  as  at  6.  In  the  latter  case  the  swinging  toward  the  dorsal 
side  becomes  less  marked  ;  hence  the  succeeding  phase  of  the  swing, 
which  carries  the  anterior  end  away  from  the  light,  is  less  pronounced  ; 


dorsal  side,  owing  to  the  decrease  in  the  illumination  of  the  anterior  end.  Thus 
the  spiral  becomes  wider,  a  and  b  showing  the  limits  of  the  swerving.  At  3  the 
normal  amount  of  swerving  is  restored,  so  that  the  new  path  is  at  an  angle  with 
the  old  one.  Now  the  organism  swerves  at  each  turn  of  the  spiral  a  short  dis- 
tance away  from  the  source  of  light,  as  at  c,  e,  g^  and  a  longer  distance  toward 
the  source  of  light,  as  at  </,/",  A,  for  the  reasons  shown  in  Fig.  23.  At  h  it  has 
in  this  manner  become  directed  toward  the  source  of  light,  and  there  is  no  fur- 
ther cause  for  swerving  more  to  one  side  than  to  the  other;  it  therefore  swims 
in  a  spiral  with  a  straight  axis  toward  the  source  of  light. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  59 

the  anterior  end  therefore  does  not  swing  so  far  in  the  direction 
away  from  the  light  as  in  the  preceding  phase  it  swung  toward  the 
light.  This  is  illustrated  at  7-8  in  Fig.  23.  But  as  a  result  of  such 
swerving  as  does  occur  the  anterior  end  is  now  (at  8)  directed  more 
away  from  the  source  of  light  than  before.  There  then  follows  a 
new  reaction,  with  increased  swerving  toward  the  dorsal  side  in  the 
next  phase  of  the  spiral  (8-1 1,  Fig.  23),  which  carries  the  dorsal  side 
toward  the  source  of  light.  Hence  the  anterior  end  swings  still  further 
toward  the  position  where  the  light  shines  directly  upon  it.  This  con- 
tinues. As  a  result  of  this  repeated  swinging  of  the  dorsal  side  slightly 
away  from  the  source  of  light  and  strongly  toward  the  source  of  light 
the  organism  gradually  changes  its  course,  continuing  to  swim  in  a 
spiral  and  to  swerve  toward  the  dorsal  side,  until  the  axis  of  the  spiral 
is  in  line  with  the  light  rays  and  the  anterior  end  is  toward  the  source 
of  light.  This  method  of  reaction  will  best  be  understood  by  a  study 
of  Figs.  23  and  24  and  their  explanation. 

Thus  the  orientation  is  gradual  and  for  a  certain  stretch  after  the 
light  has  begun  to  act  the  organism  is  not  completely  oriented.  With 
a  fairly  strong  light,  however,  the  period  of  time  required  for  complete 
orientation  is  very  slight.  Strasburger  (1878,  p.  24)  noticed  that  when 
Haematococcus  is  swimming  toward  a  source  of  weak  light  and  the 
light  is  suddenly  increased  so  as  to  reverse  the  orientation,  there  is  a 
period  of  >'  verschiedenen  Schwankungen  "  before  the  reverse  orienta- 
tion is  attained.  He  paid  little  attention  to  the  behavior  of  the 
organisms  during  this  period,  however. 

Our  account  has  been  thus  far  purely  descriptive  ;  we  have  attempted 
to  set  forth  the  events  as  they  may  be  observed,  without  trying  to 
indicate  the  causes  at  work.  We  must  now  inquire  as  to  what  is  the 
real  stimulus  and  its  method  of  action  in  producing  orientation. 

First,  we  note  that  in  becoming  oriented  Euglena  does  not  turn 
directly  toward  the  source  of  light.  As  in  the  reaction  to  other  stimuli, 
the  turning  is  throughout  toward  a  structurally  defined  side.  This 
shows  that  the  orientation  of  Euglena,  like  that  of  Stentor,  cannot  be 
accounted  for  on  the  orthodox  tropism  theory.  In  other  words,  the 
orientation  is  not  due  to  the  direct  effect  of  the  light  on  the  motor 
organs  of  the  side  on  which  it  falls.  As  in  Stentor,  orientation  may 
be  reached  by  turning  either  toward  or  away  from  the  source  of  light, 
or  in  any  intermediate  direction.  The  response  is  a  '*  motor  reaction  " 
of  a  definite  type. 

Just  what  is  the  stimulus  which  produces  this  motor  reaction.'*  All 
our  experiments  up  to  this  point  have  shown  clearly  that  this  reaction 
is  produced  by  changes  in  the  intensity  of  illumination,  and  that  a  change 
in  the  illumination  of  the  anterior  end  produces  the  reaction  as  well  as 


6o  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

does  a  change  in  the  illumination  of  the  entire  body.  Indeed,  Engel- 
mann  (18S2,  a)  showed  that  a  change  in  illumination  over  the  remainder 
of  the  body  is  inetTective  in  producing  the  reaction,  so  that  in  every  case 
the  reaction  is  due  to  the  change  in  illumination  at  the  anterior  end. 
Now,  in  the  orientation  reaction  the  conditions  are  present  for  produc- 
ing changes  of  illumination  at  the  anterior  end  of  precisely  the  character 
which  would,  in  view  of  our  other  experimental  results,  bring  about 
the  reactions  observed.  This  will  best  be  shown  by  again  examining 
in  detail  from  this  point  of  view  a  concrete  case. 

In  Fig.  23  we  will  suppose  that  the  Euglena  at  i  is  at  first  swimming 
toward  the  source  of  light.  When  it  reaches  the  position  2  the  light  is 
changed,  so  that  it  now  comes  from  the  direction  indicated  by  the 
arrows  at  the  right.  By  this  change  the  intensity  of  illumination  at 
the  anterior  end  is  decreased,  since  before  the  light  came  from  directly 
in  front  and  affected  the  entire  end,  while  now  it  falls  upon  but  one 
side.  We  know  from  other  experiments  that  as  a  result  of  such  a 
change  the  organism  reacts  by  swerving  more  toward  the  dorsal  side, 
at  the  same  time  continuing  to  revolve  on  the  long  axis.  This  is  ex- 
actly what  happens  now  ;  by  the  increased  swerving  the  organism  is 
carried  from  position  2  to  position  3.  In  this  change  the  anterior  end, 
swinging  still  farther  away  from  the  source  of  light,  is  still  less  illumi- 
nated than  before.  As  a  result  of  this  farther  decrease  in  illumination 
the  reaction  is  continued  or  increased ;  combined  with  the  revolution 
on  the  long  axis  it  carries  the  organism  successively  to  positions  4,  5 
and  6.  In  this  part  of  the  movement  the  anterior  end  becomes  pointed 
more  directly  toward  the  source  of  light,  and  is  hence  more  strongly 
illuminated ;  there  is  therefore  nothing  in  this  movement  to  cause  a 
reaction.  The  strong  swerving  toward  the  dorsal  side  then  ceases  or 
becomes  less.  But  in  the  next  phase  of  the  spiral  course  (from  7  to  8), 
there  is  necessarily  at  least  the  normal  amount  of  swerving  toward  the 
dorsal  side,  and  this  carries  the  organism  to  a  position  (8),  where 
the  intensit}'  of  the  light  acting  on  the  anterior  end  is  decreased.  As 
a  result  of  this  decrease  we  know  that  the  "'  motor  reaction  "  must  again 
be  induced  ;  the  organism  swings  then  farther  toward  the  dorsal  side* 
This  movement,  combined  with  the  revolution  on  the  long  axis,  carries 
the  Euglena  through  9  and  10  to  11.  Here  again  the  swerving  de- 
creases, because  the  change  was  from  a  less  illuminated  to  a  more 
illuminated  region.  Hence  after  reaching  12  the  Euglena  swerves  only 
a  little  away  from  the  light,  to  13  ;  then,  as  a  result  of  the  decrease  in 
illumination  at  the  anterior  end  caused  by  this  movement,  it  swerves 
far  toward  the  light,  through  14  and  15  to  16.  This  movement  causing 
greater  illumination,  the  reaction  ceases.  The  light  is  now  shining  full 
on  the  anterior  end.     The  organism  therefore  swims  forward  in  the 


REACTIONS    TO    LIGHT    IN    CILTATES    AND    FLAGELLATES.  6l 

usual  spiral  course,  in  all  phases  of  which  the  illumination  of  the  anterior 
end  is  equal.  If  the  light  came  from  the  rear  of  Euglena  i  instead  of 
from  the  direction  indicated  by  the  arrows,  the  reaction  above  described 
would  be  continued  in  the  same  way  until  the  direction  of  swimming 
was  completely  reversed. 

Thus  the  orientation  of  Euglena  in  a  continuous  light  is  due  to  the 
production  of  the  "  motor  reaction,"  with  its  turning  toward  the  dorsal 
side,  whenever  there  is  a  decrease  in  illumination  at  the  anterior  end. 

There  is  no  other  explanation  of  the  orientation,  so  far  as  I  am  able 
to  see,  that  is  in  agreement  with  all  the  facts.  At  first  one  is  tempted 
merely  to  say  that  the  subjection  of  the  anterior  end  to  shadow  pro- 
duces the  motor  reaction,  and  that  this  is  continued  until  the  anterior 
end  is  no  longer  shaded.  This  statement  is  correct  if  by  "subjection 
to  shadow"  we  mean  an  active  process,  involving  a  change  from  a 
more  illuminated  condition.  But  if  we  mean  that  darkness  as  a  con- 
tinuous, static  condition  is  the  cause  of  the  reaction,  then  considera- 
tion shows  that  this  will  not  account  for  all  the  facts.  It  leaves  out  of 
account  the  capability  of  the  organism  to  become  acclimatized  to  cer- 
tain degrees  of  light  and  shade,  and  certain  of  the  experimental  results 
are  crucial  against  it.  Thus,  suppose  the  Euglenae  are  swimming 
toward  a  source  of  weak  light,  and  a  stronger  light  is  then  allowed  to 
act  upon  them  from  another  direction.  The  anterior  end  continues  to 
receive  the  same  amount  of  light  as  before  (since  the  weak  light  still 
persists),  yet  the  organism  reacts  as  usual,  becoming  oriented  toward 
the  stronger  light.  The  motor  reaction  by  which  the  orientation  is 
brought  about  cannot  therefore  be  due  to  darkness  or  shade  (considered 
statically)  at  the  anterior  end.  On  the  other  hand,  the  case  just  men- 
tioned is  easily  understood  on  applying  the  explanation  given  above. 

Again,  it  might  be  held  that  the  reaction  is  due  in  some  way  to  the 
relative  amount  of  illumination  at  the  two  ends.  It  might  be  main- 
tained, for  example,  that  when  the  posterior  end  is  more  illuminated 
than  the  anterior,  this  difference  acts  as  a  stimulus  to  cause  the  "  motor 
reaction."  There  is,  of  course,  no  independent  evidence  in  favor  of  this 
view,  and  the  experimental  results  prove  it  to  be  incorrect.  We  have 
shown  that  the  reaction  is  produced  (i)  when  both  ends  are  equally 
stimulated,  as  when  the  light  comes  directly  from  one  side  ;  (2)  when 
neither  end  receives  light,  as  when  the  light  is  cut  off  completely.  Fur- 
ther, it  might  be  held  that  the  reaction  is  produced  when  the  anterior  end 
is  not  more  intensely  illuminated  than  the  posterior  end.  It  is,  of  course, 
a  little  difficult  to  conceive  how  so  indefinite  a  condition  could  act  as  a 
stimulus  to  a  definite  motor  reaction,  but  in  any  case  the  experiments  show 
that  this  is  not  the  real  cause  of  the  "  motor  reaction."  Thus  certain  of 
the  experiments  show  that  the  "  motor  reaction  "  is  produced  even  when 


62  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  light  is  reduced  by  the  same  amount  at  both  ends,  so  that  the  anterior 
end  is  still  more  strongly  lighted  than  the  posterior.  This  case  is 
realized  in  the  experiment  in  which  a  small  screen  is  interposed  between 
the  Euglenae  and  the  window  toward  which  they  are  swimming.  The 
light  is  thus  somewhat  decreased,  but  is  still  sufficient  to  cause  orien- 
tation. The  anterior  end  is  thus  still  lighted  more  than  the  posterior, 
yet  the  organisms  respond  with  the  ''  motor  reaction"  at  the  moment 
the  light  is  decreased.  The  same  thing  is  shown  still  more  decidedly 
in  the  experiment  described  on  page  50,  in  which  the  ''  motor  reaction  " 
is  produced  when  the  light  is  cut  ofi'  from  some  other  source  than  that 
toward  which  the  organisms  are  swimming.  In  this  case  the  propor- 
tion of  light  shining  on  the  anterior  end  is  greater  after  the  change  in 
illumination  than  before,  yet  the  ''  motor  reaction"  is  produced  at  the 
moment  the  change  takes  place. 

The  explanation  we  have  given  is,  therefore,  the  only  one  that  is  in 
agreement  with  all  the  facts,  and  it  accounts  for  every  detail  of  the  re- 
actions to  light.  The  cause  of  all  the  phenomena  of  light  reaction  in 
Euglena  is  the  fact  that  a  sudden  change  in  light  intensity  on  the  anterior 
end  induces  a  typical  "  motor  reaction."  It  is  noticeable  that  the 
reaction  is  throughout  due  to  a  dynamic  factor,  to  some  change  in  the 
relation  of  the  organism  to  the  light,  a  change  due  either  to  an  active 
alteration  of  the  environment,  or  to  a  movement  of  the  organism.  To 
static  conditions,  if  not  too  intense,  the  organism  may  soon  become 
acclimatized,  so  that  no  farther  reaction  is  caused.  The  absolute  in- 
tensity of  the  light  affects  the  reaction  only  in  so  far  as  it  determines 
whether  it  shall  be  an  increase  or  a  decrease  in  intensity  that  causes 
the  *'  motor  reaction." 

To  sum  up,  the  reaction  of  Euglena,  from  beginning  to  end,  is  ex- 
plained by  the  fact  that  a  sudden  change  in  illumination,  even  though 
slight,  causes  a  definite  motor  reaction,  the  essential  feature  of  which 
is  an  increased  swerving  toward  the  dorsal  side.  Orientation  is  brought 
about  by  the  increased  swerving  in  the  next  phase  of  the  spiral  course 
when  the  illumination  of  the  anterior  end  is  diminished,  and  by  the 
decreased  swerving  in  the  next  phase  of  the  spiral  when  the  illumination 
of  the  anterior  end  is  increased.  In  general  terms  we  can  say  that  the 
reaction  of  Euglena  to  light  is  by  the  method  of  trial  and  error.  The 
organism  tries  turning  in  many  directions ;  when  the  turning  is  such 
as  to  produce  a  decrease  in  the  illumination  of  the  anterior  end  it 
**  tries"  other  directions;  when  it  is  such  as  to  produce  increased 
illumination  of  the  anterior  end,  or  when  no  change  in  illumination 
results,  the  reaction  ceases  and  the  organism  continues  to  swim  forward 
in  that  position.  The  result  of  this  method  of  reaction  is  necessarily 
orientation  with  the  anterior  end  toward  the  source  of  light. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  63 

CRYPTOMONAS  AND  CHLAMYDOMONAS. 

Cryptomonas  ovata  is  one  of  the  organisms  studied  by  Strasburger 
(1878),  under  the  name  Chilomonas  ovata^  in  his  classical  paper  on 
reactions  to  light  in  flagellates  and  swarm-spores. 

The  specimens  studied  by  the  present  author  were  mostly  of  the 
'* young"  form,  having  pointed,  curved,  posterior  ends.  One  side  is 
strongly  convex,  while  the  other  is  less  curved,  or  is  even  concave  near 
the  posterior  end.  It  is  thus  very  easy  to  distinguish  the  two  sides  of 
the  organism  and  to  observe  their  relation  to  the  movements. 

Cryptomonas  ovata  swims  in  a  rather  wide  spiral,  with  the  more 
convex  side  toward  the  outer  surface  of  the  spiral.  In  other  words,  the 
organism  swerves  continually  toward  the  more  convex  side.  The 
response  to  usual  stimuli  is  a  strong  turn  toward  this  convex  surface ; 
this  is  easily  seen  when  the  organism  comes  in  contact  with  an 
obstacle. 

The  Cryptomonads  swim  toward  or  away  from  the  source  of  light 
under  the  same  conditions  as  Euglena,  and  gather  in  lighted  areas  in 
the  same  manner  as  does  the  organism  last  named.  They  react  to  a 
sudden  decrease  in  the  intensity  of  illumination  by  turning  toward  the 
more  convex  side.  If  the  decrease  in  intensity  is  marked,  the  organism 
turns  suddenly  for  a  long  distance,  90°  or  more,  so  that  the  course  is 
completely  changed.  If  the  stimulus  is  less  the  turning  toward  the 
more  convex  side  is  not  so  rapid,  and  since  the  revolution  on  the  long 
axis  is  continued  the  body  of  the  organism  describes  the  surface  of  a 
wide  cone  or  frustum  of  a  cone.  When  a  large  number  of  specimens 
react  in  this  way  at  the  same  time  a  peculiar  shaking  or  trembling 
appearance  is  produced;  this  is  evidently  what  Strasburger  (1878) 
called  "  Erschiitterung  "  or  *'  Zittern."  As  a  consequence  of  the  wide 
swerving,  when  the  normal  method  of  swimming  is  resumed  the  course 
lies  in  a  new  direction. 

In  all  these  respects  Cryptomonas  exactly  resembles  Euglena.  Fur- 
ther, the  organism  becomes  oriented  to  light  in  precisely  the  same  manner 
as  is  described  above  for  Euglena.  In  fact,  if  we  substitute  ''  more 
convex  side  "  for  "  dorsal  side  "  in  the  account  of  Euglena,  it  will  fit 
almost  throughout  the  reactions  of  Cryptomonas.  It  is  therefore  unnec- 
essary to  describe  the  phenomena  in  Cryptomonas  in  detail. 

A  study  was  made  also  of  the  reactions  of  a  species  of  Chlamydo- 
monas.  The  movements  of  Chlamydomonas  and  its  reactions  to  light 
resemble  those  of  Euglena  and  Cryptomonas.  But  the  organism  is  so 
small  and  the  differentiations  of  the  bodily  structure  are  so  slight  that 
I  was  unable  to  determine  the  relation  of  its  structure  to  the  spiral 
path   and  to  the  direction  of  turning  in  the  reaction.     The  oriented 


64  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

organism  reacts  to  a  decrease  in  illumination  by  a  sudden  turn  to  one 
side,  by  an  increase  in  the  width  of  the  spiral,  and  by  a  change  in  the 
course,  just  as  happens  in  Euglena  and  Cryptomonas.  The  unoriented 
organism  becomes  oriented  in  a  manner  which  is  similar  to  that  de- 
scribed above  for  the  two  organisms  just  named.  Since,  however,  I 
am  unable  to  give  the  precise  relations  of  these  movements  to  struc- 
tural differentiations  of  the  body,  a  further  account  of  details  would 
not  be  of  interest. 

GENERAL  RESULTS. 

In  summing  up  our  results  on  reactions  to  light  in  the  organisms 
studied,  there  are  two  points  of  especial  interest  which  should  be  con- 
sidered separately.  The  first  relates  to  the  nature  of  the  reaction 
produced,  the  second  to  the  nature  of  the  agent  causing  the  reaction. 

NATURE  OF  REACTION  PRODUCED  BY  LIGHT. 

As  to  the  nature  of  the  reaction  produced  by  light  there  has  been 
much  discussion.  The  orthodox  tropism  theory  is  perhaps  that  which 
has  the  greatest  number  of  adherents.  It  is  set  forth  in  detail  in  the 
paper  of  Holt  &  Lee  (1901).  According  to  this  theory  the  light  acts 
directly  on  the  motor  organs  of  the  side  on  which  it  impinges  ;  supra- 
optimal  light  causes  increase  of  the  backward  stroke  (in  the  case  of 
cilia  or  other  swimming  organs)  ;  suboptimal  light  causes  a  decrease 
in  the  backward  stroke.  The  result  is  that  the  organism  is  turned 
directly  toward  or  from  the  more  intensely  lighted  side,  and  hence 
toward  or  from  the  source  of  light.  The  diagrams  given  in  the  pre- 
ceding paper  (Figs,  i  and  2)  can  be  applied  directly  to  the  elucidation 
of  this  theory. 

In  the  experiments  on  the  ciliates  and  flagellates  set  forth  in  the 
present  paper  the  precise  method  of  reaction  was  determined  by  obser- 
vation. It  is  not  in  accordance  with  the  tropism  theory  above  set 
forth.  This  has  been  emphasized  in  detail  in  the  account  of  the 
reactions  of  Stentor,  so  that  it  need  not  be  reiterated  here.  The  reac- 
tion to  light  is  of  the  same  character  as  that  to  other  stimuli,  and  takes  the 
form  of  a  motor  reaction  in  which  the  organism  performs  a  definite 
set  of  actions.  It  first  usually  stops  or  swims  backward,  then  turns 
toward  a  structurally  defined  side,  then  continues  forward.  The 
result  is  to  change  the  course  of  the  organism.  As  a  result  of  the  con- 
tinual rotation  on  the  long  axis,  together  with  the  swerving  toward  a 
certain  side,  the  organism  comes  to  be  pointed  successively  in  every 
direction.  In  continues  to  swim  forward  in  that  direction  which  does 
not  induce  a  stimulus  to  further  swerving.  The  whole  reaction  is  a 
strongly  marked  example  of  the  type  of  behavior  which  may  be  called 
the  *'  method  of  trial  and  error." 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  65 

NATURE  OF  AGENT  CAUSING  THE  REACTION. 

(i)  The  primary  and  essential  cause  of  the  reaction  is  a  change  of 
illumination.  The  change  of  illumination  must  take  place  with  some 
suddenness,  but  need  not  be  very  great  in  amount.  The  change  in 
illumination  acts  as  an  effective  stimulus  even  though  the  degree  of 
illumination  preceding  the  change  and  that  following  it  would,  when 
acting  continuously,  produce  no  such  result.  This  is  shown  by  the 
experiments  on  Euglena,  in  which  the  light  coming  from  one  side  was 
decreased  a  certain  amount.  The  orientation  of  the  organisms  and 
their  direction  of  movement  was  the  same  before  and  after  the  change, 
but  at  the  moment  the  change  occurred  there  was  a  marked  reaction. 
Other  experiments  detailed  above  demonstrate  the  same  thing.  Further, 
the  change  in  illumination  acts  independently  of  the  direction  of  the 
rays  of  light.  This  is  shown  by  the  experiment  just  cited,  in  which 
the  effective  direction  of  the  rays  of  light  was  the  same  before  and 
after  the  reaction ;  it  is  also  shown  in  the  reaction  caused  when  the 
light  is  decreased  from  below,  in  the  case  of  Euglenae  swimming 
toward  a  window  (p.  50),  and  in  the  reaction  of  Stentor  on  passing  from 
a  shadow  to  a  lighted  region  even  when  the  animal  is  oriented  with 
anterior  end  away  from  the  light  (p.  39).  The  change  in  illumination 
acts  equally  whether  it  affects  the  entire  organism  or  only  the  anterior 
end.  The  evidence  indicates  that  in  all  cases  it  is  really  the  change  at 
the  anterior  end  which  induces  the  reaction. 

(2)  The  absolute  intensity  of  the  light  affects  the  reaction  by  deter- 
mining in  a  given  case  whether  a  reaction  shall  be  caused  by  an 
increase  or  a  decrease  in  illumination.  Through  this  action  it  also 
determines,  in  the  way  to  be  mentioned  in  the  next  paragraph,  whether 
in  a  continuous  light  the  sensitive  anterior  end  shall  be  directed  toward 
or  away  from  the  source  of  light ;  that  is,  whether  the  response  shall 
be  ''positive"  or  "negative." 

(3)  Indirectly,  and  through  the  factor  set  forth  in  paragraph  (i),  the 
direction  from  which  the  light  comes  is  a  determining  factor  in  the 
reactions.  Through  the  spiral  course  in  which  the  organisms  swim  such 
conditions  are  furnished  that  in  a  field  continuously  lighted  from  one 
side  the  sensitive  anterior  end  of  the  unoriented  organism  is  subjected 
to  repeated  changes  in  the  intensity  of  illumination.  As  a  result, 
organisms  which  respond  by  the  motor  reaction  to  an  increase  in  illu- 
mination at  the  anterior  end  must  become  oriented  with  anterior  end 
directed  away  from  the  light ;  organisms  which  react  to  a  decrease  in 
illumination  must  become  oriented  with  anterior  end  directed  toward 
the  light.  (Details  in  the  account  of  Euglena,  pp.  60,  61,  and  Figs. 
23,  24.) 


66  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  results  of  this  method  of  reacting  may  be  stated  correctly,  though 
not  completely,  as  follows :  In  a  negative  organism  light  falling  upon 
the  sensitive  anterior  end  causes  a  reaction  by  which  the  anterior  end 
is  pointed  in  many  different  directions ;  the  reaction  ceases  as  soon  as 
a  direction  is  reached  in  which  the  anterior  end  is  pointed  away  from 
the  light.  In  a  positive  organism  the  shading  of  the  sensitive  anterior 
end  produces  the  reaction  by  which  the  anterior  end  is  pointed  in  many 
different  directions ;  the  reaction  ceases  as  soon  as  the  anterior  end  is 
no  longer  shaded.*  The  reaction  is  thus  by  the  method  of  trial  and 
error ;  when  stimulated  the  organism  tries  many  different  positions, 
till  one  is  found  in  which  there  is  no  further  stimulation. 

Consideration  will  show,  I  think,  that  the  factors  producing  reaction 
to  light  in  these  lowest  organisms  are  essentially  the  same  as  in  higher 
ones,  if  man  may  be  taken  as  a  type  of  the  latter.  The  factors  are,  as 
we  have  seen,  variations  in  intensity  of  illumination,  and,  indirectly, 
the  direction  from  which  the  light  comes.  It  is  possible  that  in  man 
the  latter  factor  works  more  directly  than  in  the  infusoria ;  leaving  this 
question  out  of  consideration,  the  two  factors  are  present  in  both  cases. 
Consider  a  human  being  who  reacts  to  light  as  a  purely  physical  agent, 
not  with  regard  to  the  associations  which  it  brings  up.  In  a  dark  space 
a  gleam  of  light  is  pleasant  and  induces  movement  toward  it.  There 
is  then  a  positive  reaction  with  orientation,  but  the  orientation  is  not 
due  to  the  difference  in  intensity  of  light  on  different  parts  of  the  body, 
nor  to  its  direct  effect  on  the  motor  organs.  The  orientation  is  such  as 
to  keep  the  light  shining  on  the  more  sensitive  part  of  the  body,  the 
eyes.  An  excessively  powerful  light  is  unpleasant  and  induces  a  nega- 
tive reaction  just  as  happens  in  Euglena  ;  the  orientation  is  then  such 
as  to  keep  the  more  sensitive  part  of  the  body,  the  eyes,  away  from  the 
light.  Further,  man  is  sensitive  to  a  sudden  change  in  illumination. 
A  strong  light  bursting  from  the  darkness,  or  sudden  darkness  in  the 
midst  of  bright  light,  induces  a  marked  motor  reaction,  and  less  striking 
differences  may  produce  a  response.  Both  in  man  and  in  Euglena  the 
reaction  likewise  depends  upon  color  ;  but  with  this  phase  of  the  matter 
we  are  not  at  present  concerned. 

When  the  factors  above  set  forth  are  taken  into  consideration  certain 
peculiar  experimental  results  that  have  given  rise  to  much  discussion 
become  clearly  intelligible.  I  refer  particularly  to  the  experiments  in 
which  the  direction  of  the  light  and  the  decrease  in  intensity  of  illumi- 
nation do  not  show  the  usual  relations.  Under  ordinary  conditions 
movement  away  from  a  source  of  light  is  movement  into  a  region  of  less 


*  This  statement  is  incomplete  in  that  it  does  not  bring  out  the  fact  that  it  is 
a  change  from  light  to  shade  or  vice  versa  that  induces  the  reaction  ;  if  this  be 
understood,  the  statement  is  correct. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  67 

intensity  ;  movement  toward  the  light  into  a  region  of  greater  intensity. 
In  the  well-known  experiments  of  Strasburger  (1878)  and  others,  this 
condition  is  modified  by  passing  the  light  through  a  wedge-shaped 
prism  filled  with  a  solution  that  cuts  out  part  of  the  light. 

When  a  drop  of  water  or  a  culture  dish  is  placed  beneath  such  a 
prism,  and  the  latter  is  so  situated  that  its  surface  is  perpendicular  to 
the  light  rays,  the  intensity  of  the  illumination  is  greatest  behind  the 
thin  edge  of  the  prism,  and  thence  decreases  gradually  toward  the 
opposite  end,  while  the  rays  of  light  all  come  directly  from  above. 
Under  these  conditions  Strasburger  (1878,  p.  36)  found  that  the  positive 
swarm-spores  remained  equally  distributed  throughout  the  drop,  not 
collecting  at  the  lighter  end.  Now,  the  only  difference  between  this 
experiment  and  the  one  illustrated  in  Fig.  11  of  the  present  paper  is 
that  in  Strasburger*s  experiment  the  decrease  in  illumination  is  very 
gradual.  We  have  seen  above  (p.  52)  that  a  very  gradual  change  in 
illumination  produces  no  reaction.  Hence  the  organisms  may  wander 
from  one  side  of  the  drop  to  the  other  without  reaction,  the  difference 
in  illumination  at  two  successive  instants  never  rising  to  the  necessary 
threshold  of  stimulation.  If  the  relation  of  stimulus  to  reaction  follows 
Weber's  law,  the  result  is  just  what  we  should  expect,  provided  the 
change  in  illumination  is  sufficiently  gradual.  When  the  difference  in 
illumination  from  above  is  great,  Strasburger's  own  experiments  (/.  c, 
p.  33)  show  that  the  organisms  do  react 

On  the  other  hand,  Holt  &  Lee  (1901),  using  a  similar  prism, 
found,  under  similar  conditions,  that  the  negative  organism,  Stentor, 
does,  on  the  whole,  tend  to  gather  at  the  darker  side  of  the  drop. 
This  shows  that  the  difference  in  illumination  between  neighboring 
points  in  this  particular  experiment  was  not  below  the  threshold  of 
stimulation  for  the  organism  in  question.  If,  as  Holt  &  Lee  sup- 
pose, a  certain  amount  of  light  was  reflected  from  the  lighter  end  of 
the  vessel,  then  the  inclination  to  go  to  the  darker  side  would  be  rein- 
forced by  Stentor's  tendency  to  turn  when  the  light  falls  upon  its 
anterior  end  (see  p.  43).  The  fact  that  in  Strasburger's  experiments 
the  organisms  remained  scattered  throughout  the  drop  seems  to  indi- 
cate that  this  reflected  light  played  no  part  in  his  results. 

In  another  set  of  experiments  Strasburger  placed  his  prism  over  the 
swarm-spores  in  such  a  way  that  the  light  came  obliquely  from  the 
direction  of  the  thick  end  of  the  wedge.  If  the  positive  organisms  now 
go  toward  the  thicker  end  of  the  wedge,  they  pass  toward  the  source 
of  light,  but  into  a  region  of  decreased  illumination  ;  if  they  go  toward 
the  thin  end  they  pass  away  from  the  source  of  light,  but  into  a  region 
of  higher  illumination.     Which  will  they  choose.^ 

Strasburger  found  that  the  positive  swarm-spores  pass  toward  the 


6S  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

source  of  light,  into  the  region  of  less  illumination.  But  is  not  this 
exactly  what  we  must  expect?  His  former  experiment  showed  us  that 
under  the  prism  the  change  from  light  to  darkness  was  so  gradual  that  it 
produced  no  effect  on  the  organisms.  Hence  the  direction  from  which 
the  rays  come  is  left  to  produce  its  effect  alone,  and  it  produces  the 
usual  effect.  The  organism  reacts  in  the  usual  "  trial  and  error'*  way 
until  the  anterior  end  is  directed  toward  the  light ;  then  it  moves  in  that 
direction.  Incidentally  it  comes  into  a  region  of  less  intensity  of  light, 
though  the  decrease  is  so  slight  as  to  produce  no  effect  on  the  organism. 

Parallel  considerations  hold  for  the  negative  organism.  Under 
similar  circumstances,  if  the  variation  in  illumination  is  very  gradual, 
it  directs  its  sensitive  anterior  end  away  from  the  source  of  light  (by  the 
method  of  "trial  and  error")  and  swims  to  the  opposite  side  of  the 
drop,  incidentall}-  moving  into  a  region  of  slightly  greater  (but 
"  unperceived  ")  intensity  of  illumination.  Under  similar  conditions, 
as  we  have  seen  in  the  experiment  described  on  p.  39,  if  the  decrease 
in  illumination  is  marked,  the  animal  swims  back  into  the  shadow, 
though  in  so  doing  it  passes  toward  the  source  of  light. 

Thus  in  Strasburger's  experiments  with  the  prism  the  difference  in 
the  intensity  of  light  between  neighboring  regions  has  been  made  so 
slight  that  they  are  unmarked  by  the  organism  and  have  no  effect  upon 
it.  We  need  not  be  surprised,  therefore,  that  it  reacts  as  if  these  differ- 
ences did  not  exist ;  for  the  organism  they  do  not  exist. 

The  reaction  is  in  this  case  just  what  it  would  be  in  a  higher  organ- 
ism under  similar  conditions.  Let  us  suppose  that  the  light  stimulates 
strongly  the  sensitive  anterior  end,  the  eyes,  of  a  higher  animal  or  man  ; 
it  causes  pain  in  the  case  of  man.  There  will  be  a  tendency  (i)  to 
move  into  less  illuminated  regions ;  (2)  to  turn  the  eyes  away  from  the 
light.  Suppose  that  the  man  is  enclosed  in  a  space  into  which  the 
sun  shines  obliquely  from  above,  and  that  the  end  from  which  it  shines 
is  a  little  less  illuminated  than  the  opposite  end,  owing  to  causes  similar 
to  those  in  Strasburger's  experiment  on  the  swarm-spores.  Suppose  that 
the  man  is  at  the  end  next  the  sun.  He  cannot  know  that  the  other 
end  is  more  illuminated,  for  the  only  way  this  would  be  possible  would 
be  for  the  greater  number  of  rays  of  light  to  meet  his  eye  coming  from 
that  direction,  while  by  hypothesis  all,  or  a  much  larger  number,  of 
the  rays  are  coming  from  the  opposite  direction.  He  will,  therefore, 
turn  his  eyes  away  from  the  sun,  and  if  he  moves  will  move  toward 
the  end  away  from  the  sun.  After  having  traversed  some  distance  he 
may  observe,  if  he  is  very  discriminating,  that  he  is  as  a  matter  of  fact 
getting  into  a  region  of  somewhat  greater  illumination,  and  may  perhaps 
reason  that  the  best  thing  he  can  do  under  the  circumstances  is  to  keep 
his  eyes  turned  away  from  the  source  of  light  and  move  backward  to  the 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  69 

less  illuminated  end.  But  this  involves  the  capability  of  making  fine 
distinctions,  and  a  considerable  degree  of  intelligence  in  deciding  what  to 
do  under  the  peculiar  circumstances.  The  experiment  w^ith  the  swarm- 
spores  shows  that  they  are  incapable  of  such  fine  discrimination,  or  that 
they  are  not  sufficiently  intelligent  to  know  what  to  do  under  the  circum- 
stances. They  give  no  indication  that  they  notice  the  greater  illumina- 
tion after  having  passed  to  the  end  away  from  the  light.  Their  action 
may  be  considered  perhaps  in  a  certain  sense  as  a  "  mistake,"  but  it 
is  a  mistake  which  even  the  highest  organism  would  make,  and  which 
could  be  corrected  only  after  experience  of  its  results. 

The  results  of  our  study  of  the  light  reaction  in  ciliates  and  flagel- 
lates lead  to  conclusions  which  stand  in  sharp  contrast  with  certain 
general  conclusions  in  Radl's  recent  extensive  and  interesting  paper  on 
Phototropism  (Radl,  1903).  Radl  reaches  the  somewhat  extraordinary 
conclusion  that  light  orients  organisms  by  exercising  an  actual 
mechanical  pressure  upon  them.  This  pressure  necessarily  disturbs 
the  equilibrium  of  the  body,  which  is  then  compelled  to  change  posi- 
tion until  equilibrium  is  restored  ;  the  organism  is  then  oriented.  The 
orientation  is  a  consequence  of  the  interplay  of  two  sets  of  forces,  inner 
and  outer ;  these  cannot  be  in  equilibrium  until  the  body  has  taken  a 
certain  position  with  reference  to  the  pressure  exercised  by  the  light 
(/.  c,  pp.  151  fT.)  The  actual  turning  which  induces  orientation  must 
be  due  to  the  action  of  a  pair  of  forces  (/.  c,  p.  148).  One  of  these 
forces  is  the  pressure  produced  by  the  light. 

Orientation  produced  in  the  manner  described  in  the  present  paper 
for  the  reaction  of  ciliates  and  flagellates  to  light,  and  in  the  preceding 
paper  for  the  reaction  to  heat,  could  of  course  not  be  brought  about  in 
the  manner  supposed  by  Radl.  One  of  Radl's  chief  arguments  for  his 
view  is  that  ''no  observation  thus  far  shows  that  the  final  orientation 
is  attained  by  a  trial  or  after  an  oscillation,  but  it  takes  place  auto- 
matically"* (/.  c,  p.  141). 

The  observations  on  ciliates  and  flagellates  given  in  the  present  paper 
show  conclusively  that  the  orientation  in  these  cases  is  brought  about 
through  repeated  trials.  In  the  statement  quoted  above  Radl  has  over- 
looked certain  other  cases.  Thus  Strasburger,  as  we  have  seen  (p.  59), 
states  that  after  the  direction  of  the  light  is  changed  Haematococcus 
becomes  reoriented  "  nach  verschiedenen  Schwankungen"  (Strasbur- 
ger, 1878,  p.  24).  Radl  himself  refers  on  a  previous  page  (p.  loo)  to 
Strasburger's  observation  of  the  oscillating  movement  of  swarm-spores 
under  the  influence  of  a  variation  in  light  intensity;  Rothert  (190J, 

*"Keine  bisherige  Beobachtung  zeigt  ferner,  dass  die  schliessliche  Orientie- 
rung  etwa  durch  eine  Priifung  oder  nach  einem  Schwanken  erzielt  wurde, 
sondern  sie  folgt  automatisch." 


7©  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

p.  397)  has  called  particular  attention  to  this  as  a  possible  factor  in  the 
so-called  phototropism.  Radl  also  refers  (p.  99)  to  Exner's  view  that  in 
Copilia  the  movements  of  the  eyes  are  in  the  nature  of  a  trial  ("  abtasten") 
of  the  surroundings.  RadPs  statement,  quoted  above,  can  then  hardly 
be  considered  strictly  accurate,  even  leaving  out  of  consideration  the 
results  set  forth  in  the  present  paper.  In  many  organisms,  doubtless, 
the  reaction  to  light  is  of  that  direct  character  assumed  to  be  general  by 
Radl.  But  it  may  be  strongly  doubted  whether  this  is  what  we  may 
call  a  primitive  condition  ;  in  other  words,  whether  it  does  not  involve 
more  complicated  internal  processes  than  the  reaction  by  "  trial  and 
error."  In  any  case,  I  am  convinced  that  a  similar  reaction  to  light  by 
the  method  of  "  trial  and  error  "  will  be  shown  to  exist  in  many  other 
organisms  ;  it  is  demonstrated,  for  example,  in  Rotifera,  in  the  paper 
which  follows  the  present  one. 

Recourse  will  doubtless  be  taken  to  the  usual  refuge  when  a  sharp 
concept  has  been  defined  to  which  the  phenomena  are  not  found  to 
correspond ;  the  reactions  of  the  ciliates  and  flagellates  will  be  simply 
excluded  from  the  tropisms  and  the  definition  of  the  latter  maintained 
in  all  its  pristine  purity.  Indeed,  it  may  be  questioned  whether  the 
reactions  of  infusoria  (and  Rotatoria)  to  light  are  not  excluded  from 
phototropism  through  the  definition  given  by  Radl  on  p.  140,  what- 
ever the  method  by  which  they  are  produced.  Radl  says  "  Unter 
phototropischer  Orientierung  ist  die  Fahigkeit  der  Organismen  zu 
velstehen,  eine  feste  Einstellung  der  Achsen  des  gesamten  Korpers  in 
dem  Lichtfelde  einzunehmen."  Since  the  ciliate  or  flagellate  (or 
rotifer)  revolves  continually  on  its  long  axis,  and  swerves  continually 
toward  a  certain  side,  it  can  hardly  be  said  that  the  body  axes  have  a 
"  feste  Einstellung"  with  reference  to  the  light.  In  an  explanatory 
paragraph  Radl  says  that  in  orientation  ''immer  geht  dann  der 
Lichtstrahl  durch  die  (morphologische)  Symmetrieebene  des  Korpers" 
(/.  c,  p.  140) .  This  is  certainly  not  true  for  the  ciliate  or  flagellate  (or 
rotifer),  even  leaving  out  of  consideration  the  fact  that  in  the  former 
two  groups  the  animals  are  usually  unsymmetrical.  If  it  be  proposed, 
then,  to  exclude  the  light  reactions  of  ciliates,  flagellates,  and  rotifers 
from  the  concept  of  *'Phototropismus,"  one  can  only  agree  that  this  is 
necessary,  in  view  of  the  definitions  of  that  concept. 

But  what  is  the  value  of  a  definition  which  excludes  some  of  the  chief 
phenomena  on  which  the  concept  that  we  are  attempting  to  define  is 
based  ?  And  what  is  the  value  of  a  theory  that  depends  on  such  a 
definition  and  that  can  only  be  correct  so  long  as  we  hold  to  this 
definition.?  The  phenomena  themselves  are,  after  all,  the  final  refer- 
ence for  testing  the  correctness  of  any  definition  or  theory ;  it  is  the 
observed  phenomena  that  we  are  attempting  to  formulate  and  explain. 


REACTIONS    TO    LIGHT    IN    CILIATES    AND    FLAGELLATES.  7 1 

What  we  desire  in  the  study  of  animal  behavior  is  (i)  a  correct 
description  of  what  occurs ;  (2)  an  understanding  of  the  relation  of 
what  occurs  here  to  other  phenomena,  this  constituting  their  *'  explana- 
tion" so  far  as  an  explanation  is  possible.  Whether  the  phenomena 
when  correctly  described  and  understood  are  found  to  fall  under  some- 
one's definition  of  a  tropism  is  comparatively  unimportant ;  it  is  only 
after  such  correct  description  and  understanding  that  final  definitions 
can  be  made.  I  question  much  if  there  has  not  been  undue  haste  in 
framing  precise  definitions  for  the  phenomena  of  animal  behavior,  when 
we  know  so  little  about  the  phenomena  in  any  thorough  way.  Radl, 
I  believe,  makes  a  fundamental  error  in  attempting  to  separate  "  Pho- 
totropismus"  rigidly  from  other  reactions  to  light.  Thus,  he  repeat- 
edly cites  Euglena  as  an  example  of  an  organism  that  shows  undoubted 
phototropism.  On  page  114  he  further  cites  the  motor  reaction  of 
Euglena  when  suddenly  shaded  *  as  a  reaction  that  has  nothing  to  do 
with  phototropism.  As  I  have  shown  above,  the  two  are  really 
closely  bound  up  together ;  the  orientation  in  the  "phototropism"  is 
produced  through  this  motor  reaction.  When  the  reactions  of  organ- 
isms to  light  are  known  in  detail,  I  believe  that  many  other  reactions 
which  Radl  (p.  1 14)  attempts  to  separate  sharply  from  "  phototropism  " 
will  be  found  closely  connected  with  the  reactions  that  go  under  that 
name.  I  had  occasion  to  point  out,  in  the  paper  preceding  this,  on 
the  reactions  to  heat,  that  if  everything  which  the  organisms  do,  except 
the  orientation  itself,  is  left  out  of  consideration,  the  orientation  can  be 
accounted  for  by  any  theory  desired.  A  thorough  study  of  precisely  this 
point — the  relation  of  "phototropism"  to  the  phenomena  supposedly 
unconnected  with  it— would,  I  believe,  have  saved  Radl  from  marring 
his  otherwise  most  excellent  and  useful  contribution  to  the  study  of 
light  reactions  by  the  proposal  of  so  fantastic  a  theory  to  account  for 
the  reactions  to  light ;  a  theory  that  fairly  produces  a  shock  in  the  mind 
of  the  reader  when  it  is  reached,  coming  as  it  does  after  Radl's  thorough 
and  valuable  objective  study  of  many  of  the  phenomena  and  his  exceed- 
ingly sane,  if  somewhat  sharp,  criticism  of  other  theories.  Definition 
and  precise  classification  are  of  course  valuable  at  a  certain  stage  of 
knowledge,  but  when  carried  out  without  a  thorough  knowledge  of  the 
phenomena  dealt  with  they  may  be  a  hindrance  rather  than  a  help. 
The  thorough  knowledge  of  the  phenomena  of  animal  behavior  required 
for  this  is  far  from  existing  at  present. 


*  Radl  says  when  "  beleuchtet "  ;  this  is  evidentlj  a  slip  of  the  pen. 


THIRD    PAPER 


REACTIONS  TO  STIMULI  IN  CERTAIN 
ROTIFERA. 


73 


REACTIONS  TO  STIMULI  IN  CERTAIN   ROTIFERA, 


In  my  series  of "  Studies  on  Reactions  to  Stimuli  in  Unicellular 
Organisms  "  and  in  the  foregoing  papers  I  have  set  forth  the  reaction 
methods  of  many  infusoria  to  varied  stimuli.  The  result  has  been 
to  show  that  the  reaction  method  in  these  organisms  is  of  a  peculiar 
character,  differing  radically  from  that  required  by  prevailing  theories 
of  the  reactions  of  lower  organisms.  The  essential  nature  of  these 
reactions,  with  their  implications  as  to  the  character  of  behavior  in  the 
lower  organisms,  will  be  discussed  in  the  following  papers.  Before 
proceeding  to  this  discussion  it  is  important  to  determine  whether  the 
reaction  method  in  the  Infusoria  differs  radically  in  character  from 
that  of  Metazoa.  For  this  purpose  it  seems  well  to  select  a  group  of 
Metazoa  whose  habitat  and  mode  of  life  are  similar  to  those  of  the 
Infusoria.  In  this  way  differences  due  primarily  to  the  different  plan 
of  structure  of  the  two  sets  of  organisms  may  perhaps  be  brought  out 
without  the  complications  arising  from  different  modes  of  life. 

A  group  of  Metazoa  much  resembling  the  Infusoria  in  their  mode 
of  life  is  found  in  the  Rotatoria.  As  is  well  known,  the  members 
of  these  two  groups  are  usually  found  mingled  together.  They  are 
of  about  the  same  size,  and  both  swim  about  by  means  of  cilia.  So 
great  is  the  resemblance  in  general  habit  and  in  habitat  that  they  were 
at  first  classed  together,  all  being  given  the  name  of  Infusoria.  As 
we  know  now,  however,  they  are  really  widely  separated  in  relation- 
ship. While  the  Infusoria  are  unicellular,  the  Rotifera  are  multicellu- 
lar organisms  of  a  high  degree  of  complexity,  possessing  many  systems 
of  organs,  each  composed  of  many  cells.  In  particular,  they  have  a 
well-developed  nervous  system. 

A  comparison  of  the  behavior  of  these  two  groups  of  organisms 
should  show  us,  therefore,  whether  there  are  types  of  reaction  having 
a  high  degree  of  generality,  such  as  is  claimed  for  the  theory  of 
tropisms — types  that  may  give  a  key  to  the  behavior  of  groups  so 
widely  separated  in  relationship  as  the  two  under  consideration,  which 
are  representatives  of  the  Protozoa  and  of  Metazoa  of  a  fairly  high 
degree  of  organization. 

In  the  present  paper  I  can  attempt  to  give  an  account  of  the  behavior 
of  only  a  few  free-swimming  species,  and  that  not  in  an  exhaustive 
manner.  I  hope  to  return  to  an  extensive  study  of  the  behavior  of  this 
interesting  group,  so   as  to  develop  its  implications  for  the  theory  of 

75 


76 


THE    BEHAVIOR    OF    I.OWER    ORGANISMS. 


animal  behavior  in  general.     In  the  study  here  set  forth  observation 
— -^^  was  directed  primarily  to  the  questions  of  how 

certain  Rotifera  react  under  the  stimulus  of 
the  agencies  which  usually  give  rise  to  the  so- 
called  tropisms — light,  chemicals,  heat,  elec- 
tricity, contact,  etc. — and  to  these  questions 
the  present  account  will  be  devoted. 

The  species  whose  reactions  were  exam- 
ined belong  chiefly  to  the  loricate  group  of 
free-swimming  Rotifera,  and  include  a  num- 
ber of  species  of  the  Rattulidae,  several  species 
of  Cathypnadae,  two  or  three  species  of  Euch- 
lanis,  Plcesoma  lenticulare^  Anurcea  cochle- 
aris^  and  Brachionus  pala.  These  were 
studied  as  opportunity  offered.  In  most  cases 
the  reactions  of  any  one  species  were  not 
determined  with  relation  to  more  than  two 
or  three  classes  of  stimuli.  The  behavior  of 
AnurcEa  cochlear  is  was  examined  most  fully. 
This  species  will  be  used  as  a  type  in  describ- 
ing the  reactions.  I  have  already  given  a 
brief  account  of  the  general  reaction  type  in 
certain  species  of  the  Rattulidae  in  my  mono- 
graph of  that  group  (Jennings,  1903). 

METHOD  OF  LOCOMOTION. 

The   free-swimming   Rotifera   progress 

through  the  water  in  the  same  manner  as  the 

ciliate  infusoria.     The  cilia  in  the  Rotifera 

are  limited  to  the  anterior  end,  as  they  are 

in  the  peritrichous  infusoria.     It  is  interesting 

to  note  that  the  same  device  is  adopted  in  the 

one  group  as  in  the  other,  to  compensate  for 

irregularities  in  the  form  of  the  body,  etc., 

Fig.  25.*  which    might   result   in    swerving   from    the 

straight  course.     This  is  by  revolution  on  the  long  axis,  causing  the 

path  to  become  a  spiral  with  a  straight  axis.     In  the  Infusoria  the 


♦Fig.  25. — Spiral  path  followed  in  ordinary  swimming  by  Anurcea  cochlearis 
Gosse,  showing  different  positions  of  body  in  different  parts  of  the  course; 
a,  dorsal  surface;  ^,  left  side;  c,  ventral  surface;  d,  right  side.  The  animal 
revolves  on  its  long  axis  over  to  the  right,  thus  taking  successively  the  positions 
«,  b,  c,  d,  a,  etc.  The  large  arrow  indicates  the  general  direction  of  the  course 
followed;  the  smaller  arrows  show  direction  of  progression  in  certain  parts  of 
the  course. 


REACTIONS    TO    STIMULI    IN    CERTAIN   ROTIFERA.  77 

organism  usually  swerves  from  the  straight  line  toward  the  aboral  side  ; 
in  the  Rotatoria  it  is  usually  toward  the  dorsal  side.  Well-ordered 
forward  progression  would  therefore  not  take  place,  were  it  not  for  the 
revolution  on  the  long  axis,  converting  the  circular  course  into  a  spiral 
one.  In  the  Rotifera  the  revolution  on  the  long  axis  is,  so  far  as 
observed,  always  over  to  the  right.  These  relations  have  been  brought 
out  in  detail  in  a  previous  paper  by  the  present  author  (Jennings,  1901). 
The  spiral  path  thus  followed  by  most  of  the  free-swimming  Roti- 
fera may  be  illustrated  in  Fig.  25,  for  Anurcea  cochlear  is  Gosse.  As 
will  be  seen  from  the  figure,  the  path  followed  depends  upon  three 
factors  :  (i)  the  animal  continually  swerves  toward  its  dorsal  side  ;  (2) 
it  progresses  ;  (3)  it  revolves  on  its  long  axis.  The  result  of  these  three 
factors  is  the  spiral  course.  In  all  these  relations  the  rotifer  agrees 
with  the  infusorian. 

REACTIONS  TO  STIMULI. 

The  most  general  reaction  to  a  stimulus  in  such  a  free-swimming 
rotifer  is  an  accentuation  of  one  of  the  factors  in  this  course,  namely, 
the  swerving  toward  the  dorsal  side.  The  result  is  to  produce  a  spiral 
of  much  greater  width  than  previously  existed.  This  may  often  be 
observed  when  the  vessel  containing  the  rotifers  is  jarred.  It  is  evi- 
dent that  this  method  of  reaction  is  fitted  to  enable  the  rotifer  to  avoid 
a  small  obstacle  lying  in  its  path,  that  is,  in  the  axis  of  the  spiral. 
When  the  animal  resumes  its  former  method  of  swimming  the  axis  of 
the  spiral  lies  in  a  new  direction ;  the  course  has  thus  been  slightly 
changed. 

With  a  stronger  stimulus,  as  when  the  rotifer  strikes  against  an 
object  lying  in  its  path,  the  swerving  toward  the  dorsal  side  may  be 
still  more  pronounced,  while  the  revolution  on  the  long  axis  nearly  or 
quite  ceases.  The  result  is  that  the  organism  swings  strongly  toward 
its  dorsal  side,  and  when  the  usual  forward  swimming  is  resumed  the 
axis  of  the  spiral  lies  in  a  totally  new  direction  (Fig.  26).  It  thus 
avoids  the  obstacle,  if  the  latter  is  small ;  if  the  first  reaction  does  not 
avoid  the  obstacle  completely  the  reaction  is  repeated  until  the  course 
is  sufficiently  altered  so  that  the  rotifer  no  longer  strikes  against  the 
source  of  stimulus.  In  some  rotifers  the  increased  swerving  toward 
the  dorsal  side  is  preceded  by  swimming  backward  a  short  stretch. 

In  all  these  points  the  reaction  of  the  rotifer  agrees  even  to  details 
with  that  of  the  ciliate  infusorian.  There  is  a  difference  in  the  fact 
that  the  Infusoria  are  unsymmetrical  and  cannot  therefore  be  said  to 
swerve  toward  the  dorsal  side,  as  do  the  prevailingly  symmetrical 
Rotifera.  In  the  Rattulidas,  however,  we  have  asymmetry  of  a  char- 
acter similar  to  that  found  in  the  Infusoria. 


78 


THE    BEHAVIOR   OF   LOWER    ORGANISMS. 


We  have  dealt  thus  far  specifically  only  with  reactions  to  simple 
mechanical  stimuli,  such  as  are  presented  by  an  obstacle  in  the  path  of 


Fig.  26.* 


the  rotifer  or  by  a  simple  mechanical  jar.     This  type  of  reaction  under 
such  conditions  I  have  observed  for  Diurella  tigris  Miiller,  D.  por- 


♦  Fig.  26  is  a  diagram  of  the  reaction  of  the  rotifer  Anuraea  to  a  strong  stimulus, 
as  when  it  reaches  a  source  of  mechanical  stimulus  or  a  region  where  some 
chemical  is  dissolved  in  the  water.  From  a  to  ^  the  animal  is  unstimulated, 
hence  it  follows  the  usual  spiral  course.  At  b  it  reaches  the  stimulating  region, 
whereupon  it  turns  strongly  toward  the  dorsal  side,  following  the  arc  of  a  circle, 
from  b  to  d.  Here  it  resumes  the  usual  spiral  course  {d  to  e).  The  large  arrow 
X  shows  the  general  direction  of  progression  before  the  stimulus  was  received; 
the  arrow  J  shows  the  direction  of  progression  after  the  reaction  has  taken  place. 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


79 


cellus  Gosse,  D.  gracilis  Tessin,  and  a  number  of  other  species  of 
Rattulidae  ;  Plcesoma  lenticulare  Herrick,  Cathypna  ungulata  Gosse, 
Monostyla  bulla  Gosse,  Brachionus  pala  Ehr.,  Anurcea  cochlear  is 
Gosse,  and  A.  aculeata  Ehr. 

This  method  by  no  means  exhausts  the  possibilities  of  reaction  even 
to  a  simple  mechanical  stimulus  in  these  species.  They  may  retract 
the  head  and  cease  swimming,  may  creep  over  the  surface  of  the  object 
vv^ith  which  they  come  in  contact,  or  possibly  may  sometimes  turn  other- 
wise than  to  the  dorsal  side  when  stimulated.  Of  this  latter  point  I 
am,  however,  by  no  means  sure.  It  is  certain  that  the  typical  reaction, 
occurring  in  the  great  majority  of  cases,  is  that  described  above. 

REACTION  TO  CHEMICALS. 

The  reaction  given  when  the  organism  comes  in  contact  with  an  area 
containing  a  rather  strong 
diffusing  chemical  was 
observed  in  Aletopidia 
lepadella^  Anurma  coch- 
lear is  .^  A.  aculeata^  and 
Diurella  gracilis. 

The  method  of  experi- 
mentation was  as  follows : 
A  drop  of  water  contain- 
ing the  rotifers  was  placed 
on  a  slide.  Near  this  was 
placed  a  drop  of  N/8 
NaCl,  and  the  two  drops 
were  connected  by  a  nar- 
row neck.  The  behavior 
of  the  organisms  as  they 
came  into  the  region  of  the  neck  and  thus  in  contact  with  the  salt 
solution  was  observed  with  the  Braus-Driiner  microscope.  In  the 
species  mentioned  the  reaction  was  by  a  sudden  turn  toward  the  dorsal 
side,  by  which  the  path  of  the  animal  was  directed  away  from  the 
chemical.  The  reaction  is  thus  of  the  same  character  as  occurs  in  the 
ciliate  infusoria. 

This  manner  of  reaction  to  chemicals  is  in  both  these  groups  of 
organisms  just  what  might  be  expected  when  the  currents  caused  by 
the  cilia  are  taken  into  consideration.     In  the  ciliate,  as  I  have  shown 


Fig.  27. 


♦Fig.  27.— Diagram  of  currents  in  a  nearly  quiet  Anuraea,  showing  how  a 
diffusing  chemical  or  an  advancing  region  of  warmer  water  (represented  by  shad- 
ing), is  drawn  out  by  the  ciliary  vortex,  so  as  to  reach  the  mouth  and  the  ventral 
surface  before  affecting  other  parts  of  body. 


So  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

in  a  previous  paper  (Jennings,  1902,  a) ,  the  cilia  cause  a  current  coming 
from  the  region  in  front  of  the  organism  to  pass  along  the  oral  surface 
to  the  mouth  ;  in  this  way  the  oral  surface  comes  in  contact  with  the 
chemical  before  any  other  part  is  aflected.  It  is  not  surprising,  there- 
fore, that  the  organism  should  turn  toward  the  opposite  (aboral)  side. 

In  the  rotifera  the  conditions  are  parallel  to  those  found  in  the  ciliate. 
The  cilia  cause  a  current,  which  passes  to  the  mouth,  on  the  ventral 
surface  of  the  body  (Fig.  27).  The  solution  thus  reaches  the  ventral 
surface  first,  and  the  reaction  is,  as  might  be  expected,  a  turn  toward 
the  dorsal  side. 

It  should  be  distinctly  stated  that  this  reaction  method  is  not  universal 
in  rotifers  even  toward  chemical  stimuli.  In  some  of  the  larger  species, 
bearing  auricles,  or  with  the  ciliary  apparatus  of  a  very  complex 
character  in  other  respects,  varied  reactions  may  occur,  which  I  hope 
to  analyze  in  another  paper. 

REACTION  TO  HEAT. 

This  was  studied  in  detail  only  in  Anurcea  cochlearis.  A  large 
number  of  the  rotifers  were  mounted  in  a  shallow  trough  formed  of  a 
slide,  as  described  on  p.  12,  and  one  end  of  the  slide  was  warmed  by 
means  of  the  apparatus  shown  in  Fig.  5.  The  reactions  were  then 
observed  with  the  Braus-Driiner  stereoscopic  binocular. 

As  soon  as  a  portion  of  the  slide  has  been  warmed  above  the  optimum, 
the  rotifers  in  this  region  turn  more  strongly  than  usual  toward  the 
dorsal  side,  so  that  the  course  followed  becomes  a  very  wide  spiral  and 
the  animals  make  little  progress.  If  the  heat  is  increased  the  revolu- 
tion on  the  long  axis  ceases,  while  the  animals  swerve  still  more 
strongly  toward  the  dorsal  side  (Fig.  28),  so  that  they  swim  in  circles, 
the  dorsal  surface  being  directed  toward  the  center  of  the  circle. 
Usually  after  circling  thus  a  short  time  the  animals  begin  again  to  re- 
volve on  the  long  axis,  and  dart  forward.  The  direction  of  this  dart 
forward  seems  purely  random.  If  it  carries  the  animal  out  of  the 
heated  region  the  forward  movement  is  continued  and  the  animal 
escapes.  If  it  does  not  carry  the  animal  out  of  the  heated  region  the 
circling  toward  the  dorsal  side  is  quickly  resumed,  followed  by  another 
dart  forward.  This  is  continued  either  until  the  rotifer  passes  out  of 
the  heated  region  or  until  it  is  overcome  by  the  heat.  Usually,  if  it 
does  not  escape  soon  from  the  heated  region  the  circling  becomes 
more  rapid  and  continuous  and  is  kept  up  till  the  animal  is  destroyed 
by  the  heat. 

If  one  end  of  the  slide  is  heated  and  the  animal  approaches  the 
heated  region  from  the  opposite  end  the  reaction  is  of  the  same 
character  as  that  last  described.     As  soon  as  the  region  is  reached 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


8l 


wliere  the  heat  acts  as  an  effective  stimulus  the  animal  swerves  strongly 
toward  the  dorsal  side,  thus  beginning  to  circle,  as  shown  in  Fig.  28. 
If  this  swerving  should  continue  only  till  the  animal  had  described  a 
semicircle,  then  were  followed  by  the  forward  dart,  the  animal  would 
of  course  retrace  its  original  course  (or  one  parallel  to  it),  and  would 
thus  escape  from  the  heated  region,  as  happens  in  the  reaction  to  the 
electric  current  (Fig.  29).    But  the  reaction  to  heat  is  less  precise  than 

f 


Fig.  28.* 


this.  Usually  the  animal  makes  several  com- 
plete circles  before  darting  forward,  and  the 
direction  in  which  it  darts  seems  a  random 
one  ;  sometimes  it  is  toward  the  heated  region, 
sometimes  away  from  it,  sometimes  oblique  to 
it.  If  the  path  followed  leads  the  animal  into 
the  heated  region  the  circling  toward  the  dorsal 
side,  followed  by  the  dart  forward,  is  repeated  ;  while  if  the  path  leads 
away  from  the  heat  no  farther  reaction  is  caused  and  the  animal  escapes. 
Thus  when  a  large  number  of  the  animals  swim  toward  the  heated 
region  a  considerable  number  will  be  seen  a  little  later  to  swim  away 
again.  But  in  many  cases  the  dart  forward  carries  the  animal  still 
farther  into  the  heated  region.  These  specimens  then  begin  to  circle 
again  toward  the  dorsal  side,  and  if  the  temperature  is  high  they  may 


*  Fig.  28. — Diagram  of  a  reaction  to  heat  in  Anuraea.  The  unstimulated 
animal  at  first  advances  in  the  general  direction  shown  by  the  arrow  x,  following 
thus  the  course  a  to  e.  The  heat  is  supposed  to  be  advancing  from  the  direction 
opposite  the  arrow  x.  When  the  rotifer  reaches  the  point  e  the  heat  becomes 
effective  as  a  stimulus.  The  animal  reacts  by  turning  toward  the  dorsal  side, 
and  continues  this  so  as  to  describe  a  complete  circle,/",  ^,  A,  /,/",  etc. ;  often  it 
describes  such  a  circle  several  times.  Finally,  at  some  point  in  the  circular 
course,  as  _^,  it  resumes  the  usual  spiral  course,  following  thus  the  path  ^, /,  /. 
Its  original  course,  shown  by  the  arrow  x,  has  thus  been  exchanged  for  a  course 
having  the  general  direction  shown  by  the  arrow  v. 


$2  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

continue  this  till  death  intervenes.  In  many  cases  they  repeat  the  dart 
forward  and  some  escape  in  this  way,  while  others  do  not. 

The  reaction  of  Anuraea  to  heat  is,  therefore,  not  very  precise,  and 
many  individuals  swim  into  the  heated  region  and  are  killed.  Those 
which  escape  do  so  through  a  reaction  which  is  similar  to  that  of 
those  which  do  not ;  in  the  one  case  the  forward  movement  carries  the 
animal  out  of  the  heated  region  ;  in  the  other  it  does  not.  The  essential 
point  to  the  reaction  is  that  the  animals  when  stimulated  by  heat  change 
their  course  (through  a  "  motor  reflex").  This  changed  course  nat- 
urally is  an  advantage,  and  in  accordance  with  the  laws  of  probability 
carries  some  of  the  organisms  away  from  the  source  of  danger.  Others, 
likewise  in  accordance  with  the  laws  of  probability,  are  carried  even 
by  the  changed  course  toward  the  heated  region,  where  they  may  be 
killed  unless  a  repetition  of  the  '*  motor  reflex"  with  its  change  of 
course  carries  them  finally  away.  The  reaction  is  by  the  method 
of"  trial  and  error,"  and  is  not  always  successful. 

Altogether,  the  reaction  of  the  rotifer  Anuraea  to  heat  is  of  a  charac- 
ter similar  in  principle  to  that  of  Oxytricha  (Fig.  7,  p.  16).  The 
direction  of  turning  depends  on  an  internal  factor ;  the  reaction  takes 
the  form  of  "  a  motor  reflex,"  and  is  by  no  means  compatible  with  the 
typical  tropism  schema. 

REACTION  TO  LIGHT. 

In  light,  as  I  have  already  set  forth  in  the  account  of  the  reactions  of 
Stentor,  we  have  a  stimulating  agent  of  a  different  character  from  that 
found  in  chemicals  or  in  heat,  since  the  distribution  of  the  stimulating 
agent  is  not  afl^ected  by  the  currents  of  water  produced  by  the  motor 
organs  of  the  animal.  There  is  thus  no  reason  in  the  distribution  of 
the  stimulating  agent  to  favor  a  turning  toward  one  side  rather  than  the 
other. 

I  have  been  able  to  study  accurately  the  light  reaction  in  but  one 
rotifer,  Anurcsa  cochlearis  Gosse.  The  conditions  necessary  for 
precise  observation  of  the  nature  of  the  reaction  are  very  difficult  to 
fulfill,  and  the  usual  movements  of  the  animals  are  such  that  the  nature 
of  the  reaction  is  obscured.  As  will  be  recalled,  the  organism  is 
normally  swimming  rapidly  in  a  spiral,  continually  swerving  toward 
its  dorsal  side.  This  in  itself  is  very  confusing  when  one  attempts  to 
observe  just  how  the  organism  turns  when  stimulated.  When  light  is 
thrown  upon  it,  or  when  the  direction  of  light  falling  on  it  is  changed, 
the  response  is  usually  not  given  at  once,  and  when  it  does  occur,  as 
we  shall  see,  it  may  be  in  the  form  of  an  accentuation  of  certain  features 
of  the  normal  movement.  From  these  conditions  it  results  that  it  is 
exceedingly  difficult  to  tell,  after  a  reaction  to  light  has  clearly  occurred, 


REACTIONS    TO    STIiVlUI.I    IN    CERTAIN    HOTIFERA.  S3 

just  how  the  reaction  took  place.  Of  course,  only  sharply  defined  posi- 
tive observations  are  of  value  in  deciding  between  two  opposing  possi- 
bilities ;  hence,  although  I  have  studied  a  number  of  other  rotifers  in 
this  connection,  I  give  the  results  only  where  absolutely  sure  of  them. 
But  in  the  two  or  three  other  rotifers  I  have  examined  in  this  connection 
the  reaction  is  apparently  the  same  as  that  in  Anurcea  cochlearis^  to 
be  described  at  once. 

The  specimens  of  AnurcBa  cochlearis  studied  had  been  in  a  small 
aquarium  in  the  laboratory  some  months,  and  were  distinctly  negative 
to  light,  gathering  at  the  side  of  vessel  farthest  from  the  window.  The 
freshly  collected  animals  are,  I  believe,  usually  positive  to  light. 

These  negative  individuals  were  placed  in  a  small  flat-bottomed 
rectangular  glass  vessel,  on  a  dark  background,  in  a  dark  room.  At 
opposite  sides  of  the  vessel  and  somewhat  above  were  clamped  two 
incandescent  electric  lights,  A  and  B^  at  a  distance  of  about  lo  inches* 
in  the  manner  described  for  Stentor  (p.  41  and  Fig.  15).  One  of 
these  lights  could  be  extinguished  while  the  other  was  simultaneously 
turned  on.  In  this  way  the  direction  of  the  light  falling  on  the  rotifers 
could  be  reversed. 

When  only  one  of  the  lights,  as  A^  was  turned  on,  the  Anuraeas  all 
collected  at  the  opposite  side  of  the  vessel,  next  to  B.  When  A  was 
extinguished  and  B  turned  on,  they  turned  and  swam  in  the  opposite 
direction,  toward  A.  By  reversing  the  direction  of  the  light  while  the 
animals  were  crossing  the  vessel  their  course  could  be  reversed  while 
in  full  career. 

Focusing  the  Braus-Driiner  on  the  vessel,  and  reversing  the  lights 
when  the  animals  were  well  in  the  field  of  observation,  the  following 
could  be  observed :  Some  turned  at  once,  with  some  sharpness, 
toward  the  dorsal  side^  the  turning  continuing  until  the  direction  of 
swimming  was  reversed  and  the  animals  were  again  swimming  away 
from  the  light  (Fig.  29) .  In  these  cases  the  direction  of  turning  was 
clear  and  could  be  observed  without  great  difficulty. 

Other  individuals  continued  for  a  short  time  to  swim  in  the  same 
direction  as  before,  then  turned,  either  sharply,  as  just  described,  or 
more  slowly,  in  the  manner  to  be  described. 

Where  the  turning  was  sharp,  as  described  above,  there  was  no 
great  difficulty  in  determining  with  certainty  the  nature  of  the  reaction. 
But  in  many  cases  the  turning  took  place  more  slowly,  in  the  following 
manner  :  Either  as  soon  as  the  light  was  reversed,  or  very  soon  after, 
the  width  of  the  spiral  in  which  the  animal  was  swimming  became 
much  greater.  In  other  words,  the  animal  swerved  more  toward  the 
dorsal  side  and  progressed  less  rapidly  than  usual.  Thus  it  described 
rather  wide  circles,  and  the  swerving  toward  the  dorsal  side  increased, 


84  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

while  progression  and  revolution  on  the  long  axis  had  largely  ceased. 
After  this  circling  had  continued  for  some  time,  the  swerving  toward 
the  dorsal  side  apparently  continually  increasing,  it  was  found  that  the 
anterior  end  was  directed  away  from  the  source  of  light;  i.  c,  the 
direction  of  swimming  had  been  reversed,  and  the  animal  was  moving 
away  from  the  light. 

It  is  obviously  very  difficult  to  be  entirely  certain  of  all  that  has  hap- 
pened during  this  period  of  extensive  circling,  as  a  matter  of  direct 
observation.  But  the  evidence  seems  to  show  clearly  that  the  essential 
point  in  changing  the  course  is  the  swerving  toward  the  dorsal  side. 
The  following  facts  all  point  to  this  conclusion  :  (i)  In  the  individuals 
which  turn  at  once  it  is  possible  to  be  entirely  certain  that  the  turning 
is  toward  the  dorsal  side.  (2)  In  the  individuals  which  are  circling  it 
is  entirely  clear  that  the  swerving  toward  the  dorsal  side  is  greatly  in- 
creased, and  there  is  no  evidence  of  turning  in  other  directions.  The 
only  difficulty  is  that  one  cannot  follow  every  evolution  and  be  certain 
that  nothing  else  has  occurred.  (3)  Analysis  of  this  same  reaction 
when  given  in  response  to  other  stimuli,  where  the  conditions  are 
more  favorable  for  observation,  shows  that  it  does  consist  of  an  in- 
creased swerving  toward  the  dorsal  side,  with  a  decrease,  or  an  entire 
stoppage  for  a  time,  of  the  forward  motion.  There  is,  then,  no  reason 
to  think  that  the  reaction  contains  other  factors  when  performed  under 
the  influence  of  light.  The  reaction  is  indeed  clearly  the  same  as  that 
described  for  Euglena  on  p.  53,  and  illustrated  in  Fig.  21  ;  a  similar 
analysis  could  be  given  for  the  reaction  of  Anurasa. 

It  may  be  considered  certain,  therefore,  that  in  Anurcea  cochlearis 
the  reaction  to  light  is  similar  to  the  reaction  to  other  stimuli,  and  that 
the  orientation  is  brought  about  by  a  turning  toward  the  dorsal  side. 
The  reaction  is,  therefore,  not  due  to  the  direct  effect  of  the  light  on  the 
motor  organs ;  the  direction  of  turning  is  determined  not  by  external 
factors,  but  by  internal  factors.  The  reaction  to  light  in  the  rotifer, 
like  that  in  the  infusorian,  takes  place  by  the  method  of  ''  trial  and 
error." 

REACTION  TO  THE  ELECTRIC  CURRENT. 

A  considerable  number  of  different  species  of  the  rotifera  were  sub- 
jected to  the  continuous  electric  current  without  the  production  of  any 
characteristic  reaction.  A  current  was  used  which  could  be  graded  in 
strength  from  practically  zero  to  one  that  was  destructive,  but  no  reac- 
tion comparable  to  that  found  in  the  ciliate  infusoria  was  produced. 
On  making  or  breaking  the  current  the  animals  frequently  contracted 
quickly,  and  if  the  current  was  very  strong,  the  head  was  completely 
retracted  and  the  animal  sank  to  the  bottom.  But  there  was  no  orien- 
tation  and  the  animals  did  not  swim  toward  either  electrode.     These 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA.  85 

negative  results  were  obtained  with  several  of  the  Philodinadae  (Rotifer, 
Philodina),  some  species  of  Euchlanis  and  Salpina,  Noteus  quadri- 
cornls^  and  a  number  of  the  Rattulidae. 

In  Hydatina  senta  there  is  a  reaction  of  a  peculiar  character  which 
perhaps  furnishes  a  clue  to  the  cause  of  the  more  pronounced  reaction 
to  be  described  for  Anuraea.  With  a  current  of  moderate  strength, 
such  as  that  to  which  Paramecia  react  most  markedly,  Hydatina  shows 
no  reaction  except  when  the  head  is  directed  toward  the  anode.  But 
in  this  position  the  animal  at  once  retracts  its  cilia  and  sinks  to  the 
bottom.  Thus  a  Hydatina  may  swim  freely  about  in  water  through 
which  the  current  is  passing,  provided  it  swims  toward  the  cathode,  or 
transversely,  or  obliquely  ;  as  soon,  however,  as  it  turns  its  head  toward 
the  anode  it  stops  swimming  and  sinks  to  the  bottom.  Thus  if  an 
electric  current  is  passed  through  a  preparation  containing  a  large 
number  of  specimens  of  Hydatina,  many  will  be  seen  swimming 
toward  the  cathode  and  others  at  all  sorts  of  angles  with  the  current,  but 
none  toward  the  anode.  This  is  a  phenomenon  akin  to  what  I  have 
elsewhere  called  the  production  of  orientation  by  exclusion.  If  organ- 
isms are  prevented  from  swimming  in  any  direction  but  one,  after  a 
time,  provided  the  course  is  frequently  changed,  all  that  are  swim- 
ming will  be  found  moving  in  that  one  direction.  This  condition  is 
realized,  as  I  have  shown  in  the  first  of  these  contributions,  in  the 
reactions  of  infusoria  to  heat  and  cold.  But  in  the  reactions  of  Hydatina 
to  the  electric  current  the  "exclusion"  is  less  complete  than  in  the 
cases  just  mentioned ;  the  animal  may  swim  in  any  direction  except 
one. 

The  fact  that  the  head  is  retracted  when  directed  toward  the  anode 
and  not  in  other  positions  indicates  that  there  is  a  greater  stimulation 
at  the  anode  than  elsewhere.  This  agrees  with  much  that  is  seen  in 
the  reactions  of  infusoria  to  the  current.  After  Hydatina  has  sunk  to 
the  bottom  with  anterior  end  to  the  anode,  it  repeatedly  makes  attempts 
to  unfold  its  cilia.  But  scarcely  have  they  begun  to  operate  when 
they  are  withdrawn  again.  Each  time  that  they  are  uncovered  for  an 
instant,  however,  they  turn  the  animal  a  little  toward  its  dorsal  side. 
Thus,  after  a  considerable  number  of  attempts  to  unfold  the  cilia,  the 
head  has  become  turned  away  from  the  anode  ;  then  the  cilia  are  spread 
out  and  the  animal  goes  on  its  way  until  it  is  so  incautious  as  to  turn 
its  head  again  toward  the  anode. 

AnurcBa  cochlearis  shows  marked  electrotaxis  similar  to  that  found 
in  the  infusoria.  When  the  continuous  current  is  passed  through  a 
preparation  containing  large  numbers  of  this  species,  all  orient  quickly 
and  swim  toward  the  cathode.  They  thus  agree,  so  far,  in  their 
reaction  to  the  electric  current,  with  the  ciliate  infusoria. 


86  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  question  as  to  the  mechanism  of  the  electrotactic  reaction  in  the 
rotifer  is  of  interest  when  one  compares  the  structure  of  these  animals 
with  that  of  the  ciliate  infusoria.  The  Rotifera,  in  place  of  having  cilia 
scattered  over  the  entire  body,  are  furnished  only  with  a  group  of 
cilia  at  the  anterior  end.  In  the  Ciliata  it  is  usually  possible  to  distin- 
guish functionally  two  groups  of  cilia  (i)  the  adora/  ciUa^  about  the 
mouth  and  oral  groove,  or  at  the  anterior  end;  (2)  the  body  cilia, 
scattered  over  the  body.  The  cilia  of  the  rotifers  correspond  function- 
ally with  the  adoral  cilia  of  the  Ciliata. 

Pearl  (1900),  Wallengren  (1902-1903),  and  others  have  shown  that 
in  the  electrotactic  reaction  of  the  ciliates  the  two  sets  of  cilia  are  in 
many  cases  from  a  functional  standpoint  differently  affected.  The 
adoral  cilia  react  under  the  influence  of  the  electric  current  in  such  a 
way  as  to  tend  to  turn  the  organism  toward  the  aboral  side ;  that  is, 
they  tend  to  produce  the  same  reaction  which  the  organism  gives  in 
response  to  most  other  stimuli,  a  reaction  not  in  harmony  with  the 
tropism  schema.  The  body  cilia,  on  the  other  hand,  are  differently 
affected  on  the  different  sides  or  ends  of  the  organism  ;  those  on  the 
part  of  the  body  directed  toward  the  cathode  striking  in  one  direction  ; 
those  on  the  part  directed  toward  the  anode  striking  in  a  different 
direction.  The  result  is  that  the  organism,  through  the  action  of  the 
body  cilia,  tends  to  become  directly  oriented  in  a  way  that  is  in  harmony 
with  the  tropism  schema.  (For  details,  see  the  papers  cited.)  In  those 
ciliates  in  which  the  body  cilia  are  much  reduced,  as  in  the  Hypotricha, 
the  turning  is  determined  throughout  by  the  adoral  cilia,  so  that  the 
orientation  does  not  take  place  in  accordance  with  the  tropism  schema, 
while  in  some  others,  such  as  in  Paramecium,  the  influence  of  the  body 
cilia  is  predominant,  and  the  turning  is  in  accord  with  the  theory  of 
tropisms. 

What  conditions  shall  we  find  in  the  Rotifera,  where  the  only  exist- 
ing cilia  seem  to  agree  functionally  with  the  adoral  cilia  of  the  Ciliata  ? 

As  we  have  seen,  Anuraea  swims  as  a  rule  in  rather  wide  spirals, 
swerving  strongly  toward  the  dorsal  side  and  revolving  on  its  long  axis 
(Fig.  25).  When  the  electric  current  suddenly  acts  upon  it  the  organism 
at  once  turns  strongly  toward  the  dorsal  side,  continuing  the  turn  until 
its  head  is  brought  toward  the  cathode,  toward  which  it  swims  (Fig. 
29).  In  some  cases,  as  we  shall  see  later,  several  reactions  are  neces- 
sary for  bringing  the  body  in  line  with  the  current,  but  these  are  as  a 
rule  very  quickly  accomplished. 

If,  while  the  animals  are  swimming  toward  the  cathode,  the  current 
is  suddenly  reversed,  the  animals  again  turn  strongly  toward  the  dorsal 
side,  continuing  the  turning  until  their  position  is  reversed  and  the 
heads  point  toward  the  new  cathode  (Fig.  29).     In  many  cases  the 


REACTIONS    TO    STIMULI    IN    CERTAIN    ROTIFERA. 


87 


turning  is  continued  still  farther,  so  that  the  head  of  the  animal  de- 
scribes a  complete  circle  ;  indeed,  this  may  continue  so  that  the  animal 
whirls  around  several  times,  always  towards  the  dorsal  side.  The 
reaction  thus  far  is  the  same  as  that  produced  by  heat  (Fig.  28).  In 
reacting  to  the  electric  current  the  whirling  finally  ceases  with  ante- 


FiG.  29.* 

rior  end  directed  toward  the  new  cathode.  The  animal  then  swims 
forward  in  the  direction  so  indicated.  These  turnings,  even  when 
several  times  repeated,  require  but  a  moment,  so  that  very  soon  prac- 
tically all  the  specimens  are  swimming  toward  the  new  cathode.     The 


*  Fig.  29. — Diagram  of  method  by  which  Anuraea  becomes  oriented  to  rays  of 
light,  or  to  the  electric  current.  Taking  the  latter  for  example,  the  animal  is  at 
first  swimming  toward  the  cathode,  in  direction  indicated  by  arrow  x ;  it  thus 
follows  a  spiral  path  from  a  to  d.  At  i>  the  electric  current  is  reversed.  The 
animal  thereupon  swerves  strongly  toward  its  dorsal  side,  describing  a  semicircle, 
bj  c,  d,  until  its  anterior  end  is  directed  toward  the  new  cathode,  in  the  opposite 
direction  from  before.  It  now  follows  the  spiral  path  d  to  e,  in  the  general  direc- 
tion indicated  by  the  arrowy.  The  facts  are  similar  for  the  reversal  of  light,  or 
for  the  reaction  when  the  current  or  the  light  is  first  set  in  operation. 


S8  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

reaction  in  Anuraea  is  in  a  general  view  as  striking  and  clear-cut  as 
that  of  Paramecium. 

Thus  in  the  rotifer  Anuraea  the  orientation  to  the  continuous  elec- 
tric current  is  produced  through  a  motor  reaction,  the  essential  features 
of  which  are  determined  by  the  structure  of  the  organism.  The  organ- 
ism turns  always  toward  the  dorsal  side,  continuing  or  repeating  the 
turning  until  the  anterior  end  is  directed  toward  the  cathode.  In  these 
respects  it  agrees  with  hypotrichous  Ciliata,  where  the  direction  of 
turning  is  determined  by  the  action  of  the  adoral  cilia.  The  method 
of  reaction  is  quite  incompatible  with  the  tropism  schema. 

SUMMARY. 

The  reactions  of  those  Rotifera  of  which  an  account  is  given  in  this 
paper  take  place  in  a  manner  essentially  similar  to  the  reactions  of  the 
ciliate  infusoria. 

In  the  reactions  to  -mechanical  stimuli,  to  chemicals,  and  to  heat, 
orientation  is  not  a  striking  feature.  The  organism  turns  when  stimu- 
lated toward  a  structurally  defined  side — as  a  rule  toward  the  dorsal 
side  ;  in  this  way  it  avoids  the  source  of  stimulus. 

In  the  negative  reaction  to  light  the  organism  becomes  oriented  with 
anterior  end  directed  away  from  the  source  of  strongest  light,  but  this 
orientation  is  brought  about  in  the  same  manner  as  in  Stentor ;  the 
animal  turns  toward  the  dorsal  side  without  relation  to  the  side  on 
which  the  light  strikes  it,  and  continues  the  turning  or  repeats  it  until 
the  anterior  end  is  directed  away  from  the  source  of  light. 

To  the  continuous  electric  current  the  rotifer  Anuraea  orients  and 
swims  directly  toward  the  cathode.  The  reaction  is  brought  about  in 
the  same  manner  as  the  orientation  to  light.  When  the  current  is 
made  or  reversed  the  animal  turns  toward  the  dorsal  side  and  continues 
the  turning  until  the  anterior  end  is  directed  toward  the  cathode. 

Thus  the  direction  of  turning  is  throughout  dependent  on  an  internal 
factor,  not  primarily  on  the  way  in  which  the  stimulus  impinges  on 
the  organism.  These  reactions  of  the  Rotifera  are  thus  inconsistent 
with  a  theory  of  tropisms  which  regards  orientation  as  a  primary 
feature  of  the  reactions,  and  which  holds  that  the  action  of  the  stimu- 
lating agent  is  a  direct  one  on  the  motor  organs  of  that  part  of  the 
body  on  which  it  impinges.  The  reactions  of  the  Rotifera,  so  far  as 
described  in  the  preceding  pages,  are  brought  about,  like  those  of  the 
infusoria,  by  what  may  be  called  the  method  of  "  trial  and  error." 
The  reaction  to  any  stimulus  is  of  such  a  nature  as  to  head  the  organism 
successively  in  many  different  directions.  That  direction  is  followed  in 
which  there  is  no  stimulus  to  induce  further  turning. 


FOURTH    PAPER. 


THE  THEORY  OF  TROPISMS. 


89 


CONTENTS. 


PAGE. 


To  what  Extent  does  the  Theory  of  Tropisms  throw  Light  on  the  Behavior 

of  Lower  Organisms  ?..........  91 

Essential  Points  in  the  Theory  of  Tropisms, 92 

Reactions  to  Mechanical  Stimuli, 94 

Reactions  to  Chemicals,     .          .          ........  96 

Reactions  to  Heat  and  Cold, 98 

Reactions  to  Changes  in  Osmotic  Pressure,        ......  98 

Reactions  to  Light,    ...........  98 

Reactions  to  Gravity,          ..........  100 

Reactions  to  Electricity, 100 

R6sum6  and  Discussion, 103 

Summary, 106 

90 


THE  THEORY  OF  TROPISMS. 


TO  WHAT  EXTENT  DOES  THE  THEORY  OF  TROPISMS  THROW 
LIGHT  ON  THE  BEHAVIOR  OF  LOWER  ORGANISMS? 

The  writer  has  been  engaged  for  a  number  of  years  in  a  study,  as 
exact  and  detailed  as  possible,  of  the  behavior  and  reactions  of  a  num- 
ber of  lower  organisms.  While  the  results  obtained  have  not,  as  a 
rule,  agreed  with  the  view  that  the  behavior  of  these  organisms  is 
determined  largely  in  accordance  with  the  prevailing  theory  of  tropisms 
or  taxis,  he  has  not  discussed  their  relation  to  this  theory  in  detail. 
This  was  because  of  the  possibility  that  the  reactions  which  he  had 
studied  were  exceptional,  and  that  further  investigation  might  show 
after  all  that  the  behavior  of  the  lower  organisms  is  largely  in  accord- 
ance with  the  tropism  schema. 

At  the  present  time  the  writer  feels  that  the  work  which  he  has 
done,  or  which  has  been  done  by  those  associated  with  him,  is  of  suffi- 
cient extent  to  justify  the  pointing  out  of  certain  general  relations. 
The  reactions  of  ciliate  infusoria,  which  have  long  been  used  as  the 
types  of  illustration  for  the  tropisms,  have  been  examined  in  much 
detail,  and  less  extensive  studies  have  been  made  on  the  Bacteria 
(Jennings  &  Crosby,  1901),  the  Flagellata,  and  the  Rotifera.  The 
reactions  of  a  flatworm  have  been  studied  in  much  detail  (Pearl, 
1903),  and  researches  are  nearly  ready  for  publication,  by  investigators 
associated  with  the  author,  on  the  behavior  of  Hydra  and  of  the  leech, 
and  still  other  studies  are  under  way.  Thorough  studies,  directed  to 
the  observation  of  the  exact  movements  of  organisms  under  stimuli, 
have  recently  been  given  us  by  other  observers  also.  It  seems,  there- 
fore, worth  while  to  bring  out,  in  a  preliminary  way  at  least,  the 
relation  of  the  observations  made  to  the  prevailing  theories  of  animal 
behavior.  In  the  present  paper  this  will  be  limited  to  a  consideration 
of  the  theory  of  tropisms,  since  this  is  the  theory  most  widely  held. 

The  great  apparent  value  of  the  theory  of  tropisms  or  taxis  lies  in 
the  fact  that  it  seems  to  reduce  to  very  simple  factors  a  large  number 
of  the  most  striking  activities  of  organisms,  namely,  those  involved  in 
going  toward  or  away  from  sources  of  stimuli  of  almost  any  character. 
It  is  a  schema,  in  accordance  with  which  almost  any  movements  of  the 
organism  (not  purely  random)  might  be  supposed  to  take  place. 

91 


92  THE    BEHAVIOR    oF    LOWER    ORGANISMS. 


ESSENTIAL  POINTS  IN  THE  THEORY  OF  TROPISMS. 

The  two  essential  features  of  the  theory  of  tropisms  are  apparently 
the  following:  (i)  The  movements  of  organisms  toward  certain 
regions  and  their  avoidance  of  others  are  due  to  orientation  ;  i.  e.^  to 
a  certain  position  which  the  organism  is  forced  by  the  external  stimulus 
to  take,  and  which  leads  the  organism  toward  (or  away  from)  the 
source  of  stimulus,  without  any  will  or  desire  of  the  organism,  if  we 
may  so  express  it,  to  approach  or  avoid  this  region.  (2)  The  external 
agent  by  which  the  movement  is  controlled  produces  its  characteristic 
effect  directly  on  that  part  of  the  body  upon  which  it  impinges.  It 
thus  brings  about  direct  changes  in  the  state  of  contraction  of  the 
motor  organs  of  that  part  of  the  body  affected  as  compared  with  the 
remainder  of  the  body,  and  to  these  direct  changes  are  due  the  changes 
shown  in  the  movements  of  the  organism.  This  is  brought  out  clearly 
in  the  quotation  from  Verworn  given  on  page  8.  Loeb  (1900,  p.  7) 
sums  up  the  theory  of  tropisms  as  follows : 

The  explanation  of  them  [the  tropisms]  depends  first  upon  the  specific  irrita- 
bilitj  of  certain  elements  of  the  bodj  surface,  and,  second,  upon  the  relations 
of  symmetry  of  the  body.  Symmetrical  elements  at  the  surface  of  the  body 
have  the  same  irritability;  unsymmetrical  elements  have  a  different  irritability. 
Those  nearer  the  oral  pole  possess  an  irritability  greater  than  that  of  those 
near  the  aboral  pole.  These  circumstances  force  an  animal  to  orient  itself  toward 
a  source  of  stimulus  in  such  a  v^^ay  that  symmetrical  points  on  the  surface  of  the 
body  are  stimulated  equally.  In  this  way  the  animals  are  led  without  will  of 
their  own  either  toward  the  source  of  stimulus  or  away  from  it. 

Holt  &  Lee  (1901)  again  bring  out  our  second  point,  as  applied 
to  reactions  to  light,  with  especial  clearness : 

The  phenomena  that  have  led  to  such  an  assumption  can  be  satisfactorily 
explained  on  the  simpler  theory  that  every  ray  of  light  impinging  on  an  organism 
stimulates  at  the  -point  on  -which  it  falls^*  and  in  proportion  to  its  intensity.  ♦  *  * 
The  light  operates,  naturally,  on  the  part  of  the  animal  which  it  reaches.  The 
intensity  of  the  light  determines  the  sense  of  the  response,  whether  contractile 
or  expansive,  and  the  place  of  the  response,  the  part  of  the  body  stimulated, 
determines  the  ultimate  orientation  of  the  animal."  (Holt  &  Lee,  1901,  pp. 
479-480.) 

The  theory  of  tropisms  as  above  set  forth  depends  upon  the  reflex 
contractility  of  the  motor  organs  when  affected  by  certain  stimuli.  An 
attempt  has  been  made  to  give  it  a  still  simpler  form  in  a  recent  paper 
by  Ostwald  (1903).  Ostwald  would  omit  even  the  factor  of  reflex 
irritability,  holding  that  the  turning  which  brings  about  orientation  is 
a  mechanical  result  of  differences  in  the  internal  friction  of  the  water  or 


♦Original  not  italicized. 


THE    THEORY    OF    TROPISMS.  93 

similar  physical  differences.  The  organism  is  considered  to  continue 
to  move  its  motor  organs  in  exactly  the  same  way  after  the  external 
change  (usually  called  a  stimulus)  has  taken  place  ;  the  reason  for  turn- 
ing lies  only  in  the  different  mechanical  effect  produced  when  the  motor 
organs  act  on  a  medium  of  greater  or  less  internal  friction  than  hefore. 

It  is  difficult  to  conceive  how  anyone  having  any  acquaintance  with 
the  movements  of  organisms  could  propose  such  a  theory  as  that  of 
Ostwald,  and  indeed  this  author  states  (p.  34)  that  his  account  is  purely 
theoretical,  and  that  he  has  not  attempted  to  test  his  theory  by  experi- 
ment. We  need  not,  therefore,  dwell  upon  the  theory,  further  than  to 
point  out  the  fact  that  the  reactions  of  many  of  these  lower  organisms 
have  been  studied  thoroughly,  and  the  reflex  movements  which  they 
perform  when  subjected  to  directive  stimuli  have  been  fully  described, 
and  that  these  movements  are  entirely  incompatible  with  such  a  theory 
as  that  which  Ostwald  sets  forth.*  If  details  are  desired,  it  may  be 
pointed  out  that  all  the  observations  brought  in  the  following  that  are 
inconsistent  with  the  theory  of  tropisms  as  dependent  upon  direct 
stimulation  of  the  motor  organs  are  a  fortiori  inconsistent  with  such 
a  theory  as  that  of  Ostwald. 

We  may,  then,  turn  to  the  theory  of  tropisms  as  set  forth  in  the  above 
quotations  from  Verworn,  Loeb,  and  Holt  &  Lee.  Diagrams  illus- 
trating the  method  of  action  of  a  stimulus,  on  this  theory,  are  given  in 
the  first  of  these  contributions  (Figs,  i  and  2). 

How  far  does  this  theor}'  go  in  explaining  the  behavior  of  the  lower 
organisms. -^  "Tropisms"  has  become  the  keyword  everywhere  in 
animal  behavior  ;  it  is  supposed  to  furnish  a  ready  explanation  of  most 
of  the  puzzles  which  we  here  encounter.     How  far  is  this  justified.? 

This  question  can  be  answered  only  by  accurate  observation  of  just 
what  organisms  do   under  the  influence  of  stimuli.     The  theory  of 


♦Some  of  the  assumptions  which  Ostwald  makes  as  a  basis  for  his  physical 
analysis  of  the  swimming  of  the  lower  organisms  are  so  extraordinary  as  to 
deserve  mention  as  curiosities.  He  states,  for  example,  that  as  a  rule  the  lower 
swimming  organisms  which  exhibit  the  tropisms  show  active  movement  vertically 
only  upward;  he  thinks  it  probable  that  cases  where  they  have  been  described 
as  swimming  actively  downward  are  errors ;  that  such  downward  movement  is 
really  only  passive  falling.  Yet  everyone  who  has  worked  with  Paramecium  or 
other  Ciliata  must  know  how  far  from  the  facts  is  this  idea.  In  a  vertical  tube 
Paramecia  hasten  as  freely,  and  almost  as  frequently',  downward  as  upward. 
These  infusoria  by  no  means  collect  at  the  top  in  a  vertical  tube  so  regularly  as 
the  literature  on  geotropism  might  lead  one  to  suppose  ;  Paramecia  of  this  region 
at  least  are  almost  as  likely  to  collect  at  the  bottom  as  at  the  top.  And  there  is 
little  more  difficulty  in  Paramecium  in  distinguishing  an  active  movement  down- 
ward from  a  passive  one  than  there  is  in  man.  From  my  own  observations  I 
know  that  parallel  statements  could  be  made  for  many  other  free-swimming 
organisms,  including  Metazoa  (Rotifera  and  Crustacea),  as  well  as  Protozoa. 


^  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

tropisms  says  that  certain  definite  things  happen  in  the  change  of 
position  undergone  by  organisms  under  the  influence  of  stimuli ;  that 
the  organisms  perform  certain  acts  in  certain  ways.  The  problem  for 
the  investigator  is,  then,  Do  these  things  happen?  Does  the  organism 
perform  these  acts,  in  these  particular  ways?  These  questions  are  not 
metaphysical ;  they  can  be  answered  by  observation. 

We  have  now  before  us  a  considerable  body  of  exact  observations 
which  permit  us  to  answer  these  questions  for  a  certain  number  of 
organisms.  We  will  here  attempt  to  summarize  these  observations  so 
far  as  they  bear  upon  the  essential  points  in  the  theory  of  tropisms.  In 
particular,  we  will  ask,  (i)  Is  the  observed  behavior  brought  about 
through  orientation,  in  the  way  the  theory  of  tropisms  demands?  (2) 
Does  the  evidence  show  that  the  action  of  a  stimulus  is  directly  upon  the 
motor  organs  of  that  part  of  the  body  on  which  the  stimulus  impinges? 

REACTIONS  TO    MECHANICAL  STIMULI. 

The  reactions  to  simple  mechanical  stimuli,  as  when  the  organism 
is  touched  or  struck  by  a  hard  object  over  a  certain  definite  area  of  the 
body,  of  course  do  not  as  a  rule  present  the  conditions  required  for 
the  production  of  a  tropism,  including  a  definite  orientation.  Yet  it  is 
important  to  bring  out  certain  general  relations  shown  in  these  reactions, 
as  they  throw  light  on  the  reactions  to  stimuli  of  a  difl^erent  character. 

Most  animals  show  in  one  way  or  another  a  tendency  to  avoid  sources 
of  mechanical  shock.  In  the  higher  organisms  the  reaction  usually 
takes  the  form  of  a  turning  away  from  the  side  stimulated.  The  point 
which  needs  to  be  brought  out  here  is  that  in  ciliate  infusoria  the  direc- 
tion of  turning  depends,  not  upon  the  part  of  the  body  stimulated,  but 
upon  an  internal  factor.  Stylonychia  turns  to  the  right,  whether  stimu- 
lated on  the  right  side,  on  the  left  side,  on  the  dorsal  surface,  on  the 
anterior  end,  or  by  a  general  unlocalized  mechanical  shock  ;  and  parallel 
statements  can  be  made  for  other  infusoria.  (For  details  see  Jennings, 
1900.)  We  have  proof,  therefore,  that  the  action  of  the  stimulus  is 
on  the  organism  as  a  whole^  not  merely  upon  the  ?notor  organs  of 
that  region  of  the  body  stimulated.  Further,  it  is  clear  that  the 
response  is  a  reaction  of  the  organism  as  a  whole,  not  one  brought 
about  as  an  indirect  result  of  the  fact  that  certain  motor  organs  have 
received  a  stimulus  to  contraction.*  In  these  respects,  therefore,  the 
reactions  to  mechanical  stimuli  are  different  in  character  from  those 
assumed  to  take  place  in  the  tropisms,  and  even  in  these  unicellular 
organisms  the  processes  taking  place  must  be  more  complex  than  the 


♦This  fact  becomes  still  more  striking  when  we  recall  that  the  reaction  takes 
place  in  the  same  way  in  pieces  from  any  part  of  the  body,  from  which  any  given 
motor  organs  may  have  been  removed.     (Details  in  Jennings  &  Jamieson,  1902.) 


THE    THEORY    OF    TROPISMS.  95 

theory  of  tropisms  assumes.  Certainly  a  reaction  of  the  organism  as  a 
unit,  in  response  to  a  localized  stimulus,  is  a  phenomenon  of  a  higher 
and  more  complex  order  than  would  be  a  simple  contraction  or  other 
direct  change  in  the  motor  organs  at  the  point  stimulated. 

In  the  higher  Metazoa  the  reaction  to  a  slight  mechanical  stimulus 
at  one  side  is  usually  a  turning  either  toward  or  away  from  the  source 
of  stimulus.  So  long  as  we  do  not  analyze  the  process  further,  this 
result  might  be  interpreted  either  as  due  to  the  direct  response,  by  con- 
traction, of  the  muscles  primarily  affected  (thus  in  accordance  with  the 
tropism  theory),  or  as  a  response  of  the  organism  as  a  whole,  depend- 
ent, perhaps,  on  an  alteration  in  its  physiological  condition  brought 
about  by  the  stimulus.  The  former  interpretation  is  doubtless  much 
the  simpler.  But  we  find  in  the  unicellular  organisms  that  this  first 
interpretation  is  impossible,  and  that  we  are  forced  to  the  less  simple 
and  definite  conclusion  that  the  organism  reacts  as  a  whole.  Does  it 
not  then  become  probable  that  in  the  higher  animals  the  very  simple, 
almost  mechanical,  explanation  is  likewise  incorrect ;  that  we  have  in 
them  a  phenomenon  at  least  as  complex  as  that  found  in  the  unicellular 
animals.''  In  other  words,  should  we  conclude  that  the  reactions  in 
the  higher  Metazoa  are  simpler  and  less  unified  than  in  the  Protozoa.? 

Fortunately,  however,  we  are  not  forced  to  base  our  conclusions  on 
general  considerations.  These  reactions  have  been  minutely  studied  in 
very  few  of  the  bilateral  Metazoa,  but  Pearl  (1903)  has  given  us  a 
thorough  analysis  of  the  reactions  of  a  flatworm  (Planaria).  This 
cannot  be  taken  up  in  detail  here,  but  we  may  quote  Pearl's  con- 
clusion in  regard  to  the  positive  reaction.  This  consists  in  a  turning 
toward  the  point  stimulated,  on  a  superficial  view  a  very  simple  reac- 
tion, one  especially  well  fitted  for  explanation  on  the  theory  of  direct 
action  of  the  agent  on  the  motor  organs  of  the  region  stimulated.  Pearl 
concludes,  after  exhaustive  study,  that  the  processes  in  the  reaction  are 
as  follows : 

A  light  stimulus,  when  the  organism  is  in  a  certain  definite  tonic  condition, 
sets  off  a  reaction  involving  (i)  an  equal  bilateral  contraction  of  the  circular 
musculature,  producing  the  extension  of  the  body;  (2)  a  contraction  of  the 
longitudinal  musculature  of  the  side  stimulated,  producing  the  turning  toward 
the  stimulus  (this  is  the  definitive  part  of  the  reaction);  and  (3)  contraction  of 
the  dorsal  longitudinal  musculature,  producing  the  raising  of  the  anterior  end. 
In  this  reaction  the  sides  do  not  act  independently,  but  there  is  a  delicately 
balanced  and  finely  coordinated  reaction  of  the  organism  as  a  whole,  depending 
for  its  existence  on  an  entirely  normal  physiological  condition.     (/.  c,  p.  619.) 

Further  studies  carried  on  under  the  direction  of  the  writer,  and 
soon  to  be  published,  will  show  that  in  certain  other  bilateral  Metazoa 
it  is  equally  impossible  to  explain  the  simple  turning  toward  a  stimulus 
as  a  direct  reaction  of  the  motor  organs  of  the  part  stimulated. 


go  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

It  will  be  important  to  keep  in  mind  the  nature  of  the  reactions  to 
mechanical  stimuli,  especially  in  the  infusoria,  in  considering  the 
reactions  which  are  more  usually  classed  among  the  tropisms. 

REACTIONS  TO  CHEMICALS.* 

The  reactions  to  chemicals  have  been  studied  by  the  present  author 
and  those  associated  with  him  in  many  Ciliata,  in  certain  Flagellata, 
in  the  Bacteria,  the  Rotifera,  and  the  flatworm  ;  further  studies,  not 
yet  published,  have  been  made  on  other  organisms.'  Now,  in  regard 
to  our  first  question,  as  to  orientation,  the  following  must  be  said  : 
In  no  case  has  the  typical  reaction  been  found  to  take  the  form  of  an 
orientation,  such  as  is  demanded  by  the  theory  of  tropisms.  In  the 
ciliates,  flagellates,  and  rotifers  the  reaction  has  been  found  to  take  the 
form  of  a  "  motor  reflex,'*  a  backing  followed  by  a  turning  toward  a 
certain  structurally  defined  side,  without  regard  to  the  direction  from 
which  the  chemical  is  diffiising.  It  is  this  motor  reflex  that  causes  the 
organisms  to  collect  in  the  region  of  certain  chemicals,  and  to  avoid 
others.     (Details  in  Jennings,  "Studies,"  Nos.  I-X.) 

In  the  Bacteria  the  results  of  our  work  (Jennings  &  Crosby,  1901) 
are  in  agreement  with  those  of  Rothert  (1901).  Here,  again,  in  the 
gatherings  in  certain  chemical  solutions,  or  in  the  avoidance  of  others, 
there  is  nothing  resembling  an  orientation  in  the  lines  of  diffusion. 
The  phenomena  are  brought  about  through  a  reaction  of  the  same 
essential  character  as  the  motor  reflex  of  the  infusoria,  but  still  simpler. 
The  essential  point  is  that  the  Bacteria,  when  stimulated  chemically, 
reverse  the  direction  of  movement.     (Details  in  the  papers  just  cited.) 

In  the  flatworm  the  results  of  the  thorough  study  of  the  chemical 
reaction  by  Pearl   (1903)  maybe  given  in  that  author's  own  words: 

Planaria  does  not  orient  itself  to  a  diffusing  chemical  in  such  a  way  that  the 
longitudinal  axis  of  the  body  is  parallel  to  the  lines  of  diffusing  ions.  Its  reac- 
tions to  chemicals  are  motor  reflexes  identical  with  those  to  mechanical  stimuli. 
The  positive  reaction  is  an  orienting  reaction  in  the  sense  that  it  directs  the 
anterior  end  of  the  body  toward  the  source  of  stimulus  with  considerable  pre- 
cision, but  it  does  not  bring  about  an  orientation  of  the  sort  defined  above.  (Pearl 
loc.  cit.^  p.  701,) 

For  details,  the  original  paper  of  the  author  quoted  must  be  consulted. 
It  may  be  added  that  this  positive  reaction,  by  which  the  anterior  end 
is  directed  toward  the  source  of  stimulus,  is  identical  with  that  which 
takes  place  in  response  to  a  single  mechanical  stimulus.  This  is  analyzed 
above  (p.  95). 

Are  there  any  precise  and  detailed  observations  which  support  the 
idea  that  the  reaction  to  chemicals  is  ever  a  typical  tropism }     Before 


♦For  a  statement  of  the  theory  of  tropisms  as  applied  to  chemicals,  see  Loeb 
(1897,  p.  442)  and  Garrey  (1900,  pp.  292,  293). 


THE    THEORY    OF    TROPISMS.  97 

the  method  of  reaction  by  a  ''  motor  reflex"  had  been  described  the 
reactions  to  chemicals  had  been  referred  in  a  general  way  to  the  tropism 
schema,  but  critical  observations,  which  would  differentiate  between 
the  possibilities,  have  been  lacking.  It  is  necessary  to  use  the  greatest 
caution  in  this  matter,  as  is  shown  by  the  case  of  Chilomonas.  Garrey 
(1900),  although  he  stated  that  "a  study  of  the  mechanics  by  which 
the  organism  is  oriented  or  by  which  it  is  prevented  from  moving 
from  the  ring  into  the  stronger  acid  of  the  clear  area,  or  the  weaker 
acid  surrounding  the  ring,  proved  fruitless,"  nevertheless  concluded 
that  the  reaction  in  this  animal  was  a  case  of  typical  tropism.  In  a 
paper  published  in  the  same  number  of  the  same  journal  (Jennings, 
1900,  a),  I  showed  that  when  the  mechanism  of  the  reaction  is  worked 
out,  this  conclusion  does  not  hold,  but  that  the  reaction  takes  place 
through  a  motor  reflex,  similar  to  that  in  the  Ciliata.  In  cases,  there- 
fore, where  the  mechanism  of  the  reaction  (that  is,  the  exact  movements 
which  the  organism  performs)  has  not  been  worked  out,  conclusions  as 
to  the  nature  of  the  reaction  are  of  little  value.  The  only  case  of  which 
I  know  in  which  an  author  acquainted  with  the  method  of  response  by 
a  "  motor  reflex  "  maintains,  on  the  basis  of  observation,  a  reaction  of 
unicellular  organisms  to  chemicals  in  accordance  with  the  theory 
of  chemotropism,  is  the  case  of  Saprolegnia  swarm-spores,  as  described 
by  Rothert  (1901).  In  this  case  we  are  dealing  with  very  minute 
organisms,  and  Rothert  has  made  no  attempt  to  give  an  analysis  of  the 
relation  of  the  direction  of  turning  to  the  differentiations  in  the  body 
of  the  organism,  such  as  we  found  to  be  necessary  above  for  Chilomonas 
before  the  real  nature  of  the  reaction  could  be  determined. 

Thus  it  is  clear  that  cases  of  true  chemotropism,  in  accordance  with 
the  general  tropism  schema,  are  exceedingly  rare,  if  they  exist  at  all. 
In  almost  all  the  lower  organisms  in  which  this  matter  has  been  care- 
fully studied  it  has  been  demonstrated  that  the  reaction  to  chemicals  is 
of  a  different  type  from  that  demanded  by  the  tropism  theory. 

In  the  discussion  so  far  we  have  devoted  attention  particularly  to  the 
question  of  orientation.  When  we  examine  the  second  question  pro- 
posed, as  to  whether  the  stimulus  acts  directly  upon  the  motor  organs 
of  that  part  of  the  body  on  which  it  impinges,  we  find  the  answer 
somewhat  less  clear  than  it  was  in  the  case  of  mechanical  stimuli.  It 
is  true  that  in  the  Infusoria  and  Rotifera  the  direction  of  turning  is,  as 
in  the  case  of  mechanical  stimuli,  always  toward  a  structurally  defined 
side,  without  regard  to  the  direction  from  which  the  chemical  is  diffiis- 
ing,  so  that  at  first  view  it  seems  beyond  question  that  the  reaction  is 
no^  due  to  the  direct  action  of  the  stimulus  on  the  motor  organs  of  the 
region  on  which  it  impinges.  While  this  conclusion  is  highly  probable, 
the  observed  facts  do  not  demonstrate  it  for  chemical  stimuli  as  they 


98  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

do  for  mechanical  stimuli.  This  is  owing  to  the  fact  that  the  organism 
determines  for  itself  the  region  in  which  it  shall  be  stimulated  by  a 
chemical  in  solution,  as  well  as  the  side  toward  which  it  shall  turn. 
Now,  it  appears  that  the  side  on  which,  by  its  own  activities,  it  is,  as  a 
rule,  first  stimulated  by  a  chemical,  is  (usually,  at  least)  opposite  that 
toward  which  it  turns.  (For  details,  see  Jennings,  1902,  a.)  It  could  be 
contended,  therefore,  that  the  direction  of  turning,  in  the  case  of  chemi- 
cal stimuli,  is  a  result  of  the  direct  action  of  the  stimulating  agent  on 
the  side  stimulated.  Such  a  contention  would  have  little  general 
significance,  however,  in  view  of  the  fact  that  the  same  reaction  occurs 
as  a  response  to  various  other  stimuli,  where  this  explanation  is  quite 
impossible. 

In  certain  higher  organisms,  researches  which  were  made  under  the 
direction  of  the  writer  and  are  soon  to  appear  will  show  (i)  that  chemi- 
cal stimuli  may  produce  local  contractions  in  the  part  of  the  body  with 
which  the  chemical  comes  in  contact ;  (2)  that  these  local  contractions 
have  little  to  do  with  the  characteristic  behavior  of  the  animals  when 
subjected  to  chemicals. 

REACTIONS  TO  HEAT  AND  COLD. 

Reactions  to  heat  and  cold  have  been  fully  discussed  in  the  first  of 
these  contributions.  It  is  only  necessary,  therefore,  to  point  out  that 
the  results  are  in  almost  every  detail  parallel  with  those  for  reactions 
to  chemicals,  and  in  the  same  way  and  to  the  same  degree  inconsistent 
with  the  theory  of  tropisms.  In  organisms  higher  than  the  Infusoria 
and  Rotifera,  the  reactions  to  heat  and  cold  have  been  very  little  studied 
from  the  present  point  of  view. 

REACTIONS  TO  CHANGES  IN  OSMOTIC  PRESSURE.* 

In  the  ciliate  infusoria  the  reactions  to  differences  in  osmotic  pressure 
are  identical  with  those  to  chemicals,  save  that  the  organisms  are  much 
less  sensitive  to  osmotic  changes.  (Details  in  Jennings,  1S97  and  1899.) 
The  bearing  of  these  reactions  on  the  theory  of  tropisms  is,  therefore, 
the  same  as  was  brought  out  above  in  the  discussion  of  the  reactions  to 

chemicals. 

REACTIONS  TO  LIGHT. 

The  phenomena  shown  in  the  reactions  of  organisms  to  light  have  per- 
haps formed  the  chief  basis  for  the  theory  of  tropisms.  There  is  usually 
a  definite  orientation  shown  by  the  organisms  ;  they  move  with  the  axis 
of  the  body  parallel  with  the  light  rays  either  to  or  from  the  source  of 
light.  The  existence  of  such  orientation  forms  the  basis  of  the  theory 
of  tropisms,  and  has  been  considered  sufficient  in  itself  as  a  proof  of  the 


♦  "  Tonotaxis,"  Massart ;  "  Osmotaxis,"  Rothert. 


THE    THEORY   OF   TROPISMS.  99 

theory.  Yet  the  theory  makes  certain  definite  statements  as  to  the  cause 
of  the  orientation  and  the  way  in  which  it  is  brought  about.  These 
statements  are  open  to  observation  and  experiment.  In  most  bilateral 
animals  it  is  indeed  difficult  to  really  test  the  theory.  This  is  because 
these  animals  may  turn  directly  toward  either  side  under  the  influence 
of  light,  and  it  is  difficult  to  tell  whether  this  turning  is  due  to  the  direct 
action  of  the  light  on  the  motor  organs  or  to  a  reaction  of  the  organisms 
as  a  whole  induced  by  some  change  in  physiological  condition  brought 
about  by  the  light.  But  in  the  ciliate  infusoria  we  find  a  set  of  organisms 
so  constituted  as  to  permit  us  to  bring  the  theory  to  a  direct  test.  These 
organisms  are  unsymmetrical,  and,  as  we  have  seen,  the  usual  reaction 
is  by  a  motor  reflex  involving  a  turning  toward  a  structurally  defined 
side.  We  can,  therefore,  arrange  our  experiments  in  such  a  way  that 
the  turning  demanded  by  the  theory  of  tropisms  shall  be  the  opposite 
of  that  usually  produced  in  the  reaction  of  the  organisni  as  a  whole,  and 
observe  the  results. 

This  is  what  was  done  with  Stentor  cceruleus^  as  described  in  the 
second  of  these  contributions.  The  result,  as  we  have  seen,  is  that  the 
organism  turns  toward  a  structurally  defined  side,  without  regard  to 
what  is  demanded  by  the  theory  of  tropisms.  The  same  result  was 
obtained  with  a  number  of  flagellates  and  with  a  bilateral  Metazoan — 
the  rotifer  AnurcEa  cochlearis. 

Thus,  in  these  cases,  it  is  impossible  to  interpret  the  reactions  as  due 
to  the  direct  action  of  the  light  on  the  motor  organs  of  the  side  on 
which  the  light  impinges.  The  response  is  as  clearly  a  reaction  of  the 
organism  as  a  whole  as  is  the  reaction  to  mechanical  stimuli. 

Now  that  it  has  been  shown  that  orientation  to  light  does  occur  in 
some  cases  in  a  manner  quite  at  variance  with  the  postulates  of  the 
theory  of  tropisms,  and  this  in  organisms  widely  separated  in  structure 
and  classification,  it  can  no  longer  be  held  that  orientation  is,  fer  se, 
a  proof  of  the  tropism  theory.  In  other  words,  cases  in  which  orien- 
tation takes  place,  but  in  which  the  manner  in  which  it  is  brought 
about  has  not  been  observed,  can  not  be  assumed  as  cases  of  typical 
tropism,  due  to  the  direct  action  of  the  light  on  the  motor  organs 
of  the  side  affected.  The  reactions  of  flagellates  and  swarm-spores 
to  light,  as  described  by  Strasburger  (1878),  have  long  been  con- 
sidered types  for  the  tropisms.  In  the  second  of  these  contributions 
I  have  shown  that  in  Euglena  and  Cryptomonas  (the  latter  being  one 
of  the  organisms  studied  by  Strasburger)  the  reactions  do  not  take 
place  in  accordance  with  the  tropism  schema.  So  far  as  can  be  judged 
from  Strasburger's  account  the  reactions  of  the  swarm-spores  take  place 
in  essentially  the  same  manner  as  in  the  flagellates.  As  Rothert  (1901) 
has  pointed  out,  there  are  many  details  in  Strasburger's  account  which 


lOO  THE    BEHAVIOR    OF    LOWER   ORGANISMS. 

suggest  that  the  explanation  on  the  tropism  schema  is  incorrect.  These 
details  become  intelligible  as  soon  as  we  understand  the  real  method 
of  reaction  as  set  forth  in  the  second  of  these  contributions.  The 
assumption  that  the  reaction  is  a  typical  tropism,  when  only  the  fact  of 
orientation  is  known,  is  as  likely  to  fall  to  the  ground  in  other  cases 
as  in  those  just  mentioned. 

The  reaction  of  bacteria  to  light,  as  shown  by  Bacterium  photo- 
metricuni^  described  by  Engelmann  (1882),  is  a  typical  example  of  a 
reaction  through  a  motor  reflex  not  fitting  the  tropism  schema  at  all. 

To  sum  up,  it  is  clearly  shown  in  certain  cases  that  the  reaction  to 
light  takes  place  in  a  way  that  is  not  consistent  with  the  theory  of 
tropisms,  and  this  is  true  in  some  cases  where  a  pronounced  orienta- 
tion exists.  In  many  cases  of  orientation,  where  it  is  supposed  that 
the  theory  of  tropisms  holds,  this  is  an  assumption,  for  the  observations 
which  would  decide  the  matter  are  lacking. 

REACTIONS  TO  GRAVITY. 

In  no  case  have  the  exact  movements  of  unicellular  organisms  in 
response  to  gravity  been  worked  out  in  the  manner  in  which  this  has  been 
done  for  the  reactions  to  mechanical  stimuli,  chemicals,  heat,  light,  and 
electricity.  We  are,  therefore,  without  the  requisite  data  for  deciding 
whether  these  reactions  agree  with  the  theory  of  tropisms  or  do  not.* 

In  the  higher  organisms  in  which  the  positive  and  negative  reactions 
to  gravity  have  been  observed  (starfish,  holothurians,  flies,  insect  larvae, 
etc.),  the  conditions  are  so  complex  that,  so  far  as  I  am  able  to  see, 
observations  which  are  crucial  for  deciding  as  to  the  mechanism  of  the 
reactions  have  not  been  made  and  perhaps  can  not  be  made. 

REACTIONS  TO  ELECTRICITY. 

As  we  have  seen  in  the  third  section  of  this  paper,  the  reactions  of 
the  rotifer  to  the  continuous  electric  current  do  not  take  place  in 
accordance  with  the  theory  of  tropisms.  Anuraea  shows  a  striking 
orientation  to  the  electric  current,  swimming  directly  to  the  cathode. 
Yet  this  orientation  is  brought  about  in  a  way  that  is  quite  inconsistent 
with  the  tropism  schema.  The  reaction  takes  place  through  a  "  motor 
reflex,"  the  direction  of  turning  is  determined  by  an  internal  factor, 
and  not  by  the  way  in  which  the  current  strikes  the  organism.  The 
reaction  can  only  be  interpreted,  therefore,  as  a  reaction  of  the  organism 
as  a  whole. 


♦  In  a  forthcoming  paper  by  the  author,  based  on  work  done  since  the  above 
was  written,  it  will  be  shown  that  the  reactions  of  Paramecium  to  gravity  take 
place  in  the  same  way  as  the  reactions  to  most  other  stimuli,  so  that  they  do  not 
agree  with  the  theory  of  tropisms. 


THE    THEORY    OF   TROPISMS.  lOI 

In  the  reactions  of  the  ciliate  infusoria  to  the  constant  electric  current, 
however,  we  have,  if  nowhere  else,  phenomena  which  show  to  a 
certain  extent  clear-cut  and  undoubted  agreement  with  the  theory  of 
tropisms.  To  this  agreement  with  the  theory  of  tropisms  much  of  the 
widespread  adherence  to  the  tropism  theory  for  reactions  in  general  is 
doubtless  due.  The  reaction  of  infusoria  to  the  electric  current  is  con- 
sidered a  type  for  the  other  reactions  of  organisms. 

Yet,  in  deciding  to  what  extent  the  theoi*y  of  tropisms  helps  us  to 
understand  the  behavior  of  organisms,  certain  striking  facts  in  regard 
to  the  reaction  to  the  electric  current  need  to  be  taken  into  considera- 
tion.    These  are  the  following : 

(i)  The  reaction  to  the  electric  current  never  takes  place  in  nature. 
As  has  been  repeatedly  pointed  out,  the  electric  reaction  is  a  product 
of  the  laboratory ;  it  is  a  reaction  which  the  organism  never  gives 
under  normal  conditions.  This  being  true,  it  should  not  be  made  the 
type  for  reactions  in  general  unless  it  can  be  shown  clearly  that  the 
characteristic  features  in  the  effects  of  electricity  on  organisms  are 
present  also  in  the  effects  of  other  agents.  Otherwise  we  may  fall  into 
the  same  error  that  would  exist  if  we  considered  the  contortions  of  a 
person  who  had  grasped  the  electrodes  of  a  powerful  battery  as  a  type 
of  human  behavior  in  general. 

(2)  But  examination  shows  that  the  characteristic  features  of  the 
effect  of  electricity  on  organisms  are  not  present  in  the  case  of  other 
stimuli.  The  electric  current,  as  the  experiments  of  Kiihne  (1864) 
and  Roux  (1891)  have  shown,  polarizes  the  cell.  That  is,  it  divides 
it  into  halves,  differing  in  chemical  reaction.  One  half,  in  the  case 
described  by  Kiihne,  had  apparently  an  acid  reaction,  the  other 
half  an  alkaline  reaction.  In  its  effects  on  free-swimming  organisms 
a  similar  polarity  is  shown.  In  Paramecium,  for  example,  the  cilia 
on  one  half  of  the  body  (where  the  current  is  entering)  are  caused  to 
take  a  certain  position,  while  those  on  the  other  half  (where  the  cur- 
rent is  leaving)  take  the  opposite  position.  No  other  agent  known 
produces  these  polar  effects^  either  chemically  or  in  the  effect  on  the 
motor  organs.  Yet  it  is  to  exactly  these  effects  that  the  orientation 
which  makes  this  reaction  the  type  for  the  tropism  theory  is  due. 

■If  other  agents  produce  these  effects  why  are  they  not  known  and 
described  }  There  is  no  great  difficulty  in  observing  these  effects  with 
the  use  of  the  electric  current.  Just  as  exact  studies  have  been  made 
of  the  reactions  to  other  stimuli ;  yet,  so  far  as  I  am  aware,  no  one 
has  ever  described  any  other  stimulus  as  giving  these  characteristic 
polar  effects.  On  the  contrary,  the  reactions  to  other  stimuli  are  well 
known  not  to  show  these  characteristic  phenomena. 

Since,  therefore,  the  characteristic  phenomena  of  the  reaction  to  the 


I02  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

electric  current  are  not  found  in  the  reactions  to  other  stimuli,  it  seems 
a  perversion  to  make  the  electric  reaction  a  type  for  all  others.  The 
reaction  of  the  infusoria  to  the  electric  current  takes  in  its  characteristic 
features  a  unique  position  amongthereactionsof  the  organism,  requiring 
special  explanation. 

(3)  In  the  response  of  the  infusoria  to  the  electric  current  there 
appears  also  the  same  type  of  reaction  that  occurs  as  a  response  to  other 
stimuli,  but  obscured  by  the  phenomena  peculiar  to  the  effects  of  the 
current. 

This  fact,  that  the  reaction  to  the  electric  current  is  of  a  dual  char- 
acter, that  the  peculiar  effects  of  the  current  are,  as  it  were,  superposed 
upon  the  usual  method  of  reaction,  is  not  usually  so  clearly  recognized 
as  it  deserves  to  be. 

If  the  constant  current  is  passed  through  a  preparation  containing 
large  numbers  of  some  species  of  the  Hypotricha,  as  Stylonychia  or 
Oxytricha,  it  will  be  found  that  the  animals,  practically  without  excep- 
tion, attain  their  orientation  by  turning  toward  the  right  side,  thus 
reacting  as  they  would  to  any  other  stimulus.  Further,  if  after  they 
are  oriented  the  direction  of  the  current  is  reversed,  the  animals  all, 
without  exception,  attain  their  new  orientation  (with  anterior  ends  in 
the  opposite  direction)  by  whirling  toward  their  right  sides.  Thus,  so 
far,  the  reaction  to  the  electric  current  is  identical  with  that  to  other 
stimuli,  and  the  direction  of  turning  is  determined  by  an  internal  factor, 
not  by  the  way  in  which  the  current  strikes  the  organism.  In  these 
respects  the  Hypotricha  agree  with  the  Rotifera. 

But  exact  observation  shows  that  in  the  Hypotricha  there  is  another 
factor  involved  in  the  reaction.  The  characteristic  polarizing  effect  of 
the  current  appears  in  its  action  on  the  motor  organs  that  are  distributed 
over  the  body  surface  ;  those  on  one  half  of  the  body  strike  in  one 
direction,  those  on  the  other  half  in  the  opposite  direction.  Part  of 
these  motor  organs,  therefore,  assist  in  turning  the  organism  in  its  usual 
way  (to  the  right)  ;  part  oppose  this  turning.  The  result  is  that  in 
certain  positions  the  turning  to  the  right  is  opposed  by  the  stroke  of  a 
large  number  of  cilia,  so  that  the  turning  takes  place  more  slowly  than 
usual.  Nevertheless,  in  the  Hypotricha,  the  determining  factor  in  the 
reaction  to  the  electric  current  is  almost  throughout  the  same  as  in 
the  reaction  to  other  stimuli ;  the  direction  of  turning  is  determined  by 
internal  factors,  as  a  reaction  of  the  whole  organism,  not  by  the  direction 
in  which  the  current  strikes  or  passes  through  the  organism.  (Details 
in  the  work  of  Pearl,  1900.) 

If  in  place  of  one  of  the  Hypotricha  we  experiment  with  an  infusorian 
in  which  the  cilia  cover  closely  the  whole  surface  of  the  body,  as  Para- 
mecium, the  peculiar  polarizing  effect  of  the  current  on  the  cilia  of  the 


THE    THEORY    OF    TROPISMS.  IO3 

two  halves  of  the  body  becomes  much  more  powerful,  because  the 
number  of  cilia  affected  in  this  way  is  much  greater.  The  result  is  that 
it  almost  alone  determines  the  nature  of  the  reaction.  The  direction  of 
turning  is,  therefore,  determined  by  the  way  in  which  the  current  strikes 
the  body,  as  required  by  the  theory  of  tropisms.  But  it  should  be 
recognized  that  this  is  by  no  means  universal  among  the  infusoria ;  in 
doubtless  fully  as  many  cases  the  direction  of  turning  is  determined, 
even  under  the  electric  stimulus,  by  an  internal  factor. 

This  peculiar  dual  character  of  the  reaction  to  the  electric  current — 
one  strong  factor  being  due  to  the  inherent  tendency  of  the  organism 
to  turn  in  a  certain  definite  way,  without  regard  to  the  way  in  which 
the  stimulating  agent  impinges  upon  it — has  been  studied  in  detail  in 
recent  contributions  by  Pearl  (1900),  Putter  (1900),  and  Wallengren 
(1902  and  1903).  We  may  perhaps  compare  it,  without  indicating  any 
similarity  in  details,  to  the  behavior  of  a  person  who  has  taken  hold  of 
the  electrodes  from  a  powerful  induction  coil.  He  attempts  in  various 
ways  to  free  himself  from  the  electrodes.  This  may  be  compared  with 
the  attempt  of  the  infusorian  to  perform  its  usual  reaction  to  strong 
stimuli.  He  also  undergoes  involuntary  contortions,  due  to  the  action 
of  the  electricity  on  his  muscles  ;  these  may  be  compared  with  the  pecu- 
liar effect  of  the  electric  current  on  the  cilia  of  the  infusoria,  causing 
them  to  strike  in  opposite  directions  on  the  two  halves  of  the  body. 

Putting  all  together,  we  are  not  justified  in  taking  the  reaction  of  the 
infusoria  to  the  electric  current  as  a  general  type  for  the  reactions  of 
the  lower  organisms,  because  in  its  characteristic  features  it  differs 
from  all  the  other  known  reactions.  Yet  it  is  exactly  these  unique 
features  that  bring  it  into  (partial)  agreement  with  the  tropism  schema. 

RESUME  AND  DISCUSSION. 

We  have  thus  passed  in  review  the  reactions  of  a  large  number  of 
lower  organisms  to  the  commoner  stimuli,  so  far  as  they  are  known 
from  exact  observations.  We  have  found  that  as  a  rule  they  do  not  fit 
into  the  tropism  schema.  In  the  reactions  to  mechanical  stimuli,  to 
heat  and  cold,  to  chemicals,  to  changes  in  osmotic  pressure,  orientation 
is  not  a  primary  or  striking  factor  of  the  reaction ;  when  a  common 
orientation  of  a  large  number  of  organisms  occurs,  it  is  a  secondary 
result,  due  to  the  fact  that  the  organisms  are  prevented  from  swimming 
in  any  other  direction.  In  the  reaction  to  light  orientation  is  a  strik- 
ing feature ;  but  the  orientation,  in  certain  precisely  investigated  cases 
at  least,  is  brought  about  in  a  manner  which  is  inconsistent  with  the 
tropism  schema.  In  the  reaction  to  gravity  the  precise  reaction  method 
has  not  been  worked  out.  Only  in  the  reaction  to  the  constant  electric 
current  do  we  have  in  some  organisms  a  partial  agreement  in  principle 


104  "T"^    BEHAVIOR    OF   LOWER    ORGANISMS. 

with  the  requirements  of  the  tropism  theory,  and  this  agreement  is  due 
to  an  effect  on  the  organism  in  the  production  of  which  the  electric 
stimulus  is  unique,  so  far  as  known.  In  none  of  the  reactions  which 
have  been  thoroughly  worked  out,  except  partially  in  the  reaction  to 
the  electric  current,  are  the  phenomena  to  be  explained  on  the  view 
that  the  result  is  due  to  the  direct  action  of  the  stimulating  agent  on  the 
motor  organs  of  the  part  of  the  body  on  which  it  impinges.  In  the 
reactions  to  mechanical  stimuli  and  to  light,  and  in  the  reactions  to 
the  electric  current  in  some  animals,  this  view  is  absolutely  disproved. 
The  direction  in  which  the  organism  turns  is,  in  all  the  well  known 
reactions  of  unicellular  organisms  and  rotifers  (except  in  a  portion  of 
the  reactions  to  the  electric  current) ,  determined  by  an  internal  factor, 
and  predictable  from  the  structure  of  the  organism  without  any  know- 
ledge of  the  direction  from  which  the  stimulating  agent  is  to  come. 

We  should  perhaps  consider  here  a  modification  of  the  original  form 
of  the  tropism  theory  that  has  been  proposed  by  some  authors.  This 
is  in  regard  to  the  assumption  that  the  stimulating  agent  acts  directly 
on  the  motor  organs  upon  which  it  impinges.  For  this  it  is  sometimes 
proposed  to  substitute  the  view  that  the  action  of  the  stimulating  agent 
is  directly  on  the  sense  organs  of  the  side  on  which  the  stimulus  im- 
pinges, and  only  indirectly  on  the  motor  organs  through  their  nervous 
connection  with  the  sense  organs.  When  thus  modified  the  theory,  of 
course,  loses  its  simplicity  and  its  direct  explaining  power,  which  made 
it  so  attractive.  In  order  to  retain  any  of  its  value  for  explaining  the 
movements  of  organisms,  it  would  have  to  hold  at  least  that  the  connec- 
tions between  the  sense  organs  and  motor  organs  are  of  a  perfectly 
definite  character,  so  that  when  a  certain  sense  organ  is  stimulated  a 
certain  motor  organ  moves  in  a  certain  way.  When  we  find,  as  we 
do  in  the  flatworm  (see  the  following  paper),  that  to  the  same  stimulus 
on  the  same  part  of  the  body,  under  the  same  external  conditions,  the 
animal  sometimes  reacts  in  one  way,  sometimes  in  another,  the  tropism 
theory,  of  course,  fails  to  supply  a  determining  factor  for  the  behavior. 

But  can  we  explain  the  reaction  methods  of  the  infusoria  and  other 
animals  which,  as  set  forth  above,  are  inconsistent  with  the  tropism 
theory  in  its  original  form,  on  the  basis  of  the  modification  of  this 
theory,  set  forth  in  the  last  paragraph.?  While  in  the  infusoria  the 
assumption  of  nervous  connections,  etc.,  is  inadmissible,  we  may 
waive  that  objection  and  answer  the  question  proposed  from  an  analysis 
of  the  obsei-ved  phenomena.  In  Stentor  or  in  Stylonychia,  for  example, 
we  find  that  the  usual  reaction  to  all  classes  of  stimuli  is  by  backing, 
then  turning  toward  the  aboral  side  ;  in  some  of  the  rotifers  by  turning 
toward  the  aboral  (dorsal)  side.  To  simplify  matters,  we  may  take 
into  consideration  only  the  turning  toward  the  aboral  side.     This  turn- 


THE    THEORY   OF   TROPISMS.  IO5 

ing  is  due  to  a  certain  method  of  movement  of  certain  motor  organs. 
In  the  rotifers  it  is  the  coronal  cilia  which  accomplish  the  turning, 
while  in  the  infusoria  we  know  that  the  adoral  cilia  are  concerned  in 
the  movement.  We  may  take  the  coronal  or  adoral  cilia,  then,  as  rep- 
resentativ^e  of  the  organs  active  in  the  turning.  For  convenience  we 
may  designate  these  active  organs  simply  as  x. 

Now,  when  the  animal  is  stimulated  on  the  right  side,  we  find  that 
the  motor  organs  x  move  in  a  definite  way.  On  the  tropism  theory  we 
would  conclude,  therefore,  that  the  portion  of  the  right  side  stimulated 
has  nervous  connection  with  the  organs  x.  But  we  find  also  that  when 
stimulated  on  the  left  side,  the  oral  side,  or  the  aboral  side,  the  organs 
X  move  in  exactly  the  same  manner.  In  other  words,  we  find  that  it 
does  not  depend  on  the  side  stimulated  what  organs  respond,  as  re- 
quired by  the  tropism  theory.  This  theory,  then,  in  its  modified  form, 
is  of  no  more  service  for  these  cases  than  in  its  original  form.  The 
responses  in  the  animals  which  we  have  considered  must,  therefore, 
be  conceived  as  reactions  of  the  organism  as  a  whole,  and  due  to  some 
physiological  change  produced  by  the  stimulus,  not  as  the  result  of 
direct  changes  in  certain  motor  organs  when  they  or  the  parts  with 
which  they  are  most  closely  connected  are  locally  affected  by  a  stimu- 
lating agent.  The  facts  show  that  the  parts  act  in  the  service  of  the 
wliole,  not  that  the  action  of  the  whole  is  due  to  the  more  or  less  inde- 
pendent irritability  and  activity  of  the  parts. 

Thus  the  facts  brought  out  show  that  the  theory  of  tropisms  is  not 
of  great  service  in  helping  us  to  understand  the  behavior  of  these  lower 
organisms.  On  the  contrary,  the  reactions  of  these  organisms  seem 
as  a  rule  thoroughly  inconsistent  in  principle  with  the  fundamental 
assumptions  of  the  theory. 

The  facts  brought  out  above  are  based  on  a  study  of  what  is,  of  course, 
a  comparatively  small  number  of  organisms.  They  rest  chiefly  on  an 
extensive  study  of  the  ciliate  infusoria,  with  less  thorough  examination 
of  bacteria,  flagellata,  rotifers,  and  a  few  higher  organisms.  Doubtless 
in  organisms  which  are  made  up  of  many  parts  which  are  less  firmly 
bound  together  into  a  unified  body  than  in  those  considered,  we  may 
find  greater  independence  of  action  in  the  parts.  This  seems  to  be  the 
case,  for  example,  in  the  sea  urchin,  with  its  numerous  independently 
acting  spines,  pedicellariae,  tube  feet,  etc.  In  this  animal  Von  Uexkiill 
(1900,  1900,  a)  concludes  from  his  extensive  study  of  the  reactions  that 
many  features  in  the  behavior  which  seem  at  first  view  to  be  activities 
of  the  animal  as  an  individual  are  really  due  to  the  independent  reac- 
tions of  the  parts,  so  that  he  can  say  that  while  in  walking,  in  the  case 
of  the  dog,  ''  the  animal  moves  its  legs  ;  in  the  sea  urchin  the  legs  move 
the  animal."     This  method  of  behavior  has  a  general  agreement  with 


I06  THE    BEHAVIOR    OP    LOWER    ORGANISMS. 

what  is  demanded  by  the  tropism  schema,  though  when  we  come  to 
details  of  the  behavior  of  the  organs  themselves,  this  theory  seems 
unsatisfactory,  even  in  the  sea  urchin. 

Such  organisms  as  the  sea  urchin,  composed  anatomically  and  physio- 
logically of  many  parts,  each  acting  almost  as  an  independent  animal, 
are  certainly  less  common  than  more  unified  animals,  such  as  we  find 
in  the  Infusoria,  the  Rotifera,  the  flatworms,  etc.  For  this  reason, 
therefore,  it  has  seemed  worth  while  to  sum  up  the  real  relations  of  the 
behavior  of  these  organisms  to  the  tropism  theory.  The  unicellular 
animals  are  precisely  those  on  which  the  prevailing  theories  of  tropisms 
or  taxis  have  by  many  writers*  been  chiefly  based.  With  the  demon- 
stration that  the  behavior  of  these  organisms  (as  well  as  of  many  higher 
ones),  is  for  the  greater  part  inconsistent  with  the  tropism  theory,  per- 
haps a  large  portion  of  the  foundation  for  its  acceptance  as  a  general 
formula  for  the  chief  features  in  the  behavior  of  lower  animals  is  cut 
from  beneath  it. 

In  the  following  paper,  on  the  part  played  in  behavior  by  physio- 
logical conditions  of  the  organism,  we  shall  find  other,  and,  as  it  seems 
to  me,  still  more  cogent,  reasons  for  holding  the  tropism  theory  inade- 
quate to  account  for  the  determining  factors  in  the  behavior  of  most 
lower  organisms. 

SUMMARY. 

The  foregoing  paper  consists  of  a  review  of  the  behavior  of  Ciliata, 
Flagellata,  Bacteria  ;  of  Rotatoria  and  certain  other  Metazoa,  so  far 
as  known  from  exact  observation  of  their  actions  when  stimulated, 
with  a  view  to  determining  how  far  the  prevailing  theory  of  tropisms 
aids  us  in  understanding  the  behavior  of  lower  organisms. 

The  following  are  considered  the  essential  points  in  the  prevailing 
theory  of  tropisms  ;  (i)  That  orientation  is  the  primary  factor  in  deter- 
mining the  movements  of  organisms  into  or  out  of  certain  regions,  or 
their  collection  in  or  avoidance  of  certain  regions ;  (2)  that  the  action 
of  the  stimulus  is  directly  upon  the  motor  organs  of  that  part  of  the 
organism  upon  which  the  stimulus  impinges,  thus  giving  rise  to  changes 
in  the  state  of  contraction,  which  produce  orientation. 

The  reactions  of  the  organisms  above  named  are  then  reviewed  to 
determine  in  how  far  there  is  agreement  with  these  essential  points  in 
the  theory  of  tropisms.     The  following  are  pointed  out: 

The  reactions  to  mechanical  stimuli,  to  chemicals,  to  heat  and  cold, 
and  to  variations  in  osmotic  pressure  have  been  described  in  detail,  and 
it  is  found  that  orientation  is  not  a  primary  nor  a  striking  factor  in 
them.     The  response  in  all  these  cases  is  produced  through  a  "  motor 


♦This,  however,  is  not  true  of  Loeb. 


THE    THEORY    OF    TROPISMS.  IO7 

reaction"  consisting  usually  of  a  movement  backward,  followed  by  a 
turning  toward  a  structurally  defined  side.  The  direction  of  turning  is 
thus  determined  by  internal  factors. 

In  the  reaction  to  light  orientation  is  a  striking  factor,  but  the  orienta- 
tion is  not  primary,  being  due  to  the  production  of  the  same  "  motor 
reaction"  described  in  the  last  paragraph.  The  method  of  orientation 
is  incompatible  with  the  idea  that  orientation  is  due  to  the  direct  action 
of  the  stimulus  upon  the  motor  organs  of  the  part  of  the  body  on  which 
the  light  impinges,  for  orientation  occurs  by  turning  always  toward  a 
certain  structurally  defined  side,  without  regard  to  the  part  of  the  body 
struck  by  the  light.  The  turning  may,  therefore,  be  toward  or  away 
from  the  source  of  light,  or  in  any  intermediate  direction.  In  any  case 
it  is  continued  or  repeated  until  the  anterior  end  is  directed  away  from 
the  source  of  light,  when  it  ceases. 

The  exact  method  of  reaction  to  gravity  has  not  been  worked  out  by 
direct  observation. 

In  the  reaction  to  the  electric  current  the  reaction  method  of  the 
rotifer  is  by  a  "  motor  reflex,"  and  is  hence  inconsistent  with  the  tro- 
pism  schema.  In  the  Infusoria  there  is  a  partial  (but  only  partial) 
agreement  with  the  requirements  of  the  tropism  theory.  But  this 
partial  agreement  with  the  theory  is  due  to  certain  peculiar  effects  of 
the  electric  current  which  are  not  known  to  be  produced  by  any  other 
stimulus.  Hence  the  reaction  to  the  electric  current,  far  from  being  a 
type  for  reactions  in  general,  is  a  unique  phenomenon,  demanding 
special  explanation. 

The  general  conclusion  is  drawn  that  the  theory  of  tropisms  does 
not  go  far  in  helping  us  to  understand  the  behavior  of  the  lower  organ- 
isms ;  on  the  contrary  their  reactions,  when  accurately  studied,  are,  as 
a  rule,  inconsistent  with  its  fundamental  assumptions.  The  responses 
to  stimuli  are  usually  reactions  of  the  organisms  as  wholes,  brought 
about  by  some  physiological  change  produced  by  the  stimulus ;  they 
can  not,  on  account  of  the  way  in  which  they  take  place,  be  interpreted 
as  due  to  the  direct  effect  of  stimuli  on  the  motor  organs  acting  more 
or  less  independently.  The  organism  reacts  as  a  unit,  not  as  the  sum 
of  a  number  of  independently  reacting  organs. 


FIFTH   PAPER 


PHYSIOLOGICAL  STATES  AS  DETERMINING 

FACTORS  IN  THE  BEHAVIOR  OF 

LOWER  ORGANISMS. 


109 


CONTENTS. 


PAGE. 

Nature  and  Evidences  of  Physiological  States,    .         .         .         .         .         .     iii 

Physiological  States  in  the  Protozoa  (Stentor  as  a  Type),  .         .         .112 

Physiological  States  in  the  Lower  Metazoa  (the  Flatworm  as  a  Type),  .  115 
Changes  in  the  Sense  of  "  Tropisms  "  and  other  Reactions,       .  .  .      117 

Changes  in  the  Sense  of  Reactions  with  Changes  in  the  Intensity  of  the 

Stimulus, 118 

Interference  of  Stimuli,      .         .         .         .         .         .         .         .         .         .119 

Spontaneous  Movements,  .........     120 

Methods  of  Causing  Changes  in  Physiological  States,        ....     120 

Nature  of  Reactions  to  Stimuli, 121 

Physiological  States  in  the  Behavior  of  Higher  Animals  as  compared  with 

those  in  Lower  Organisms,  ........     124 

Summary,  ............     126 

no 


PHYSIOLOGICAL  STATES  AS  DETERMINING 
FACTORS  IN  THE  BEHAVIOR  OF  LOWER 
ORGANISMS. 


NATURE  AND  EVIDENCES  OF  PHYSIOLOGICAL  STATES. 

In  studying  the  behavior  of  the  lower  organisms  the  units  of  obser- 
vation, the  factors  to  which  especial  attention  has  been  paid  have  been 
usually  the  iropisms  and  reflexes.  These  factors  may  be  considered 
as  determined  mainly  (i)  by  the  action  of  external  agents  on  the 
organism  ;   (2)  by  the  structure  of  the  organism. 

An  examination  of  the  results  of  the  study  of  reactions  in  the  lower 
animals  up  to  the  present  time  shows,  I  believe,  that  we  must  recog- 
nize another  set  of  factors  in  their  behavior,  of  equal  importance  with 
either  of  those  already  named.  This  set  of  factors  may  be  characterized 
by  the  general  term  physiological  states. 

By  physiological  states  we  mean  the  varying  internal  physiological 
conditions  of  the  organism,  as  distinguished  from  permanent  anatomical 
conditions.  Such  different  internal  ph3^siological  conditions  are  not 
directly  perceptible  to  the  observer,  but  can  be  inferred  from  their 
results  in  the  behavior  of  the  animal.  These  results  are  of  so  marked 
a  character  that  the  inference  to  different  physiological  conditions  is 
beyond  question. 

In  the  study  of  tropisms  and  reflexes  a  considerable  number  of 
instances  have  been  brought  to  light  of  changes  in  the  reaction  methods, 
such  as  can  be  attributed  only  to  changed  physiological  conditions. 
Some  of  these  cases  will  later  be  considered  in  detail  in  this  paper. 
Comparatively  few  investigations  on  the  behavior  of  lower  organisms 
have  been  published  in  which  attention  has  been  consciously  directed 
to  these  physiological  states,  and  in  most  of  these  the  matter  has  been 
taken  up  rather  incidentally.  We  may  mention  as  instances  of  papers 
dealing  more  or  less  with  this  aspect  of  the  matter  that  of  Hodge  and 
Aikins  (1895)  on  Vorticella,  those  of  Von  Uexkiill  (1S99,  1900,  1900,  a, 
1903)  on  the  sea  urchin  and  on  Sipunculus,  my  own  on  the  behavior 
of  fixed  Infusoria  (Jennings,  1902),  and  that  of  Pearl  (1903)  on  the 
flatworm.  In  the  study  of  higher  organisms  attention  has  of  necessity 
been  largely  directed  to  the  phenomena  determined  by  varying  physio- 
logical states,  as  these  play  a  striking  part  in  the  behavior. 

In  the  present  paper  an  attempt  will  be  made  to  collect  and  analyze 

a  number  of  the  known  cases  showing  the  influence  of  physiological 

states  on  the  behavior  of  the  lower  animals,  pointing  out  some  of  their 

bearings  on  the  theories  of  behavior. 

Ill 


112  THE   BEHAVIOR    OF   LOWER    ORGANISMS. 


PHYSIOLOGICAL  STATES  IN  THE  PROTOZOA  (STENTOR 
AS  A  TYPE). 

We  will  take  up  first  the  lowest  organisms  in  which  the  matter  has 
been  studied  in  detail,  that  is,  the  unicellular  animals.  These  are  of 
special  interest  in  view  of  their  entire  lack  of  a  nervous  system.  As 
the  best-known  case  we  may  take  the  behavior  of  Stentor.  This  has 
been  described  in  full  in  a  former  paper  by  the  present  author  (Jennings, 
1902,  a) ;  for  details  this  paper  may  be  consulted. 

When  a  quiet,  extended  Stentor  is  stimulated  by  lightly  touching  it 
or  the  support  to  which  it  is  attached  with  a  rod,  it  reacts  by  giving  a 
definite  reflex,  that  is,  by  contracting  into  its  tube. 

After  this  has  taken  place  once  or  twice  we  find  that  the  Stentor  no 
longer  reacts  as  before.  All  the  external  conditions  remain  the  same  ; 
the  stimulus  applied  is  the  same.  Nevertheless,  the  Stentor  does  not 
react.  Therefore,  we  must  conclude  that  the  Stentor  itself  has  changed. 
Its  physiological  condition  is  now  difierent  from  what  it  was  originally. 
What  the  nature  of  the  change  in  its  condition  is  we  do  not  know,  save 
in  the  fact  that  the  Stentor  in  this  second  condition  does  not  react  as 
does  the  Stentor  in  the  first  condition.  For  the  sake  of  convenience 
we  may  number  the  different  physiological  conditions,  in  order  that  we 
may  determine,  if  possible,  how  varied  these  conditions  are.  We  will 
call  the  physiological  condition  of  the  undisturbed  extended  Stentor, 
before  the  stimulation.  No.  i,  or  the  first  condition.  The  condition 
in  which  the  Stentor  no  longer  responds  to  the  slight  stimulus  we  will 
call  No.  2. 

We  may  frequently  distinguish  still  a  third  condition  in  the  behavior 
under  this  simple  stimulus.  At  first  the  Stentor  reacts  by  contraction 
(condition  i).  Then  it  no  longer  reacts  (condition  2).  Later,  or  in 
other  cases,  it  may  react  to  the  stimulus,  but  by  a  different  method 
from  the  first  reaction.  It  now  bends  over  to  one  side  when  touched 
with  the  rod.  As  set  forth  in  my  previous  paper,  ''The  impression 
made  on  the  observer  is  very  much  as  if  the  organism  were  at  first 
trying  to  escape  a  danger,  and  later  merely  trying  to  avoid  an  annoy- 
ance." As  conditioning  this  third  method  of  behavior,  when  all  out- 
ward conditions  are  the  same,  we  must  postulate  a  third  physiological 
state  differing  from  the  other  two  ;  this  we  may  call  condition  No.  3. 

We  may  thus  distinguish  at  least  three  different  physiological  states  in 
the  reactions  to  very  weak  stimuli,  where  the  initial  marked  response 
becomes  a  weak  one  or  disappears.  We  may  now  analyze  in  the  same 
way  the  behavior  under  stimuli  of  a  different  character,  when  there  is 
a  series  of  reactions  which  may  be  considered  of  increasing  rather  than 


PHYSIOLOGICAL    STATES    AS    DETEKMININCi    FACTORS.  II3 

of  decreasing  intensity.  Such  a  case  is  that  described  in  my  previous 
paper,  when  water  mixed  with  carmine  particles  is  allowed  to  reach 
the  disk  of  Stentor. 

The  first  physiological  condition  is  again  No.  i — that  of  the  undis- 
turbed extended  Stentor.  In  this  condition  the  organism  does  not 
respond  to  the  stimulus  at  all.  After  the  stimulus  has  continued 
for  some  time,  the  organism  does  respond  by  turning  into  a  new 
position.  We  have,  therefore,  a  new  physiological  condition.  The 
reaction  in  this  case  is  the  same  as  that  given  in  condition  No.  3, 
described  above.  Whether  the  condition  now  existing  is  the  same  as 
in  the  former  case  we  do  not  know ;  as  we  have  no  positive  evidence 
to  the  contrary,  we  will  number  it  3  also. 

Next,  after  several  repetitions  of  this  reaction,  the  organism  responds 
in  a  still  different  manner,  by  momentarily  reversing  the  ciliary  current. 
Since  the  stimulus  and  other  external  conditions  remain  the  same,  the 
organism  itself  must  have  changed.  We  may  call  its  physiological 
condition  at  the  present  time  No.  4. 

Next,  the  animal  contracts  strongly  and  repeatedly.  This  is  clearly 
the  result  of  a  still  different  physiological  condition  which  we  may  call 
No.  5. 

After  thus  contracting  repeatedly  we  find  that  the  organism  remains 
contracted  much  longer  than  it  did  at  first.  It  is  thus  now  in  a  new 
physiological  condition,  which  we  may  designate  as  No.  6. 

Finally,  it  breaks  its  attachment  to  the  bottom  of  the  tube  and  swims 
away  through  the  water.  Probably,  therefore,  we  should  distinguish 
a  seventh  physiological  state,  corresponding  to  this  reaction.  It  is 
possible,  however,  that  the  breaking  of  the  attachment  is  due  to  the 
strong  contractions  which  characterize  condition  No.  6,  so  that  the 
evidence  for  a  seventh  physiological  condition  is  not  unmistakable,  and 
it  may  be  omitted  from  consideration. 

We  are  able  to  distinguish  clearly,  therefore,  in  the  study  of  these 
two  sets  of  reactions,  at  least  six  different  physiological  states.  In  each 
of  these  states  Stentor  is  a  different  organism,  so  far  as  its  reactions  to 
stimuli  are  concerned.  Clearly,  then,  the  external  stimuli  and  the 
permanent  anatomical  configuration  of  the  body  are  by  no  means  the 
deciding  factors  in  the  behavior.  These  factors,  in  the  reaction  series 
last  described,  permit  at  least  five  different  methods  of  behavior. 
Which  of  these  methods  is  actually  realized  depends  not  on  the  quality 
or  intensity  of  the  stimulus,  nor  on  the  anatomical  structure  of  the 
organism,  but  on  its  physiological  condition. 

I  do  not  wish  to  imply  that  I  hold  that  the  six  different  physiological 
states  above  distinguished  are  sharply  defined,  separate  things.  On 
the  contrary,  it  is  much  more  probable  that  the  different  physiological 


114  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

conditions  form  a  continuum.  We  can,  by  taking  sections,  as  it  were, 
at  different  intervals,  distinguish  at  least  six  actually  different  condi- 
tions ;  but  doubtless  there  exists  every  possible  gradation  from  one  to 
another,  so  that  still  other  actually  different  conditions  could  be  distin- 
guished if  we  had  criteria  for  separating  them.  By  careful  analytical 
experiments  the  number  of  different  physiological  conditions  clearly 
recognizable  could  doubtless  be  increased. 

In  other  unicellular  organisms  doubtless  a  condition  of  affairs  may 
be  found  similar  to  that  set  forth  above  for  Stentor.  Hodge  &  Aikins 
(1895)  showed  that  the  reactions  of  Vorticella  vary  with  its  physio- 
logical condition.  In  the  same  paper  (Jennings,  1902,  a)  in  which 
the  behavior  of  Stentor  was  described,  I  have  shown  that  in  various 
other  fixed  infusoria  (Carchesium,  Epistylis,  etc.)  the  behavior  like- 
wise depends  upon  physiological  states  of  the  organism.  In  the 
free-swimming  infusoria  this  has  not  been  shown  to  be  true,  at  least  to 
any  such  extent.  There  may  two  grounds  for  this.  Firstly,  it  is  proba- 
ble that  in  the  free-swimming  infusoria  the  behavior  is  actually  less 
varied  than  in  the  fixed  species.  A  single  motor  reaction  usually 
removes  them  from  the  action  of  the  stimulus  causing  it,  so  that  there 
is  no  reason  for  a  recourse  to  other  methods  of  reaction,  as  occurs  in 
Stentor.  Secondly,  in  the  free-swimming  infusoria  it  is  difficult,  almost 
impossible,  to  observe  continuously  the  reactions  of  a  given  single 
individual.  This  difficulty  could  doubtless  be  met  by  proper  methods 
of  experimentation,  and  if  this  were  done  it  can  hardly  be  doubted  that 
a  dependence  of  the  reactions  on  the  physiological  states  of  the  organism 
would  be  found  here  also.  Indeed,  we  have  indirect  evidence  that  this 
is  true  in  the  case  of  Paramecium,  in  work  already  published.  Thus, 
in  one  of  my  earlier  papers  (1899,  a,  p.  374)  I  called  attention  to  the 
fact  that  Paramecia  from  different  cultures  often  vary  exceedingly  in 
their  reaction  to  a  given  solution  of  a  chemical.  Still  more  pertinent 
to  the  point  under  consideration  is  the  fact,  described  in  the  first  of  my 
studies  (Jennings,  1897),  as  well  as  in  the  recent  paper  of  Putter  (1900), 
of  the  great  difference  in  the  reaction  of  Paramecia  and  other  fixed 
infusoria  when  in  contact  with  a  solid,  as  contrasted  with  their  reaction 
when  not  thus  in  contact.  As  this,  however,  may  be  interpreted  as  an 
interference  of  two  stimuli,  a  discussion  of  the  point  is  reserved  until 
later.  A  study  of  individual  specimens  of  some  of  the  larger  Hypo- 
tricha,  such  as  Stylonychia,  from  the  point  of  view  of  changes  in  reaction 
methods  with  changes  in  physiological  condition,  would  doubtless  bring 
forth  interesting  results. 

Even  in  the  lower  unicellular  organisms,  the  Rhizopoda,  similar 
dependence  of  the  method  of  reaction  on  the  physiological  state  of 
the  organism  is  known  to  exist.     Thus  Rhumbler  (1898,  p.  241)  has 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  II5 

observed  that  Atnoeba  verrucosa  may  at  first  begin  to  ingest  an  Alga 
filament,  then  later,  before  the  ingestion  is  complete,  the  filament  may 
be  ejected.  This  involves  a  change  in  the  physiological  condition  of 
the  Amoeba  ;  otherwise  it  would  not  now  reject  a  certain  object  which 
it  before  ingested. 

PHYSIOLOGICAL  STATES  IN  THE  LOWER  METAZOA  (THE 
FLATWORM  AS  A  TYPE). 

Passing  now  to  the  Metazoa,  we  find  in  the  flatworm,  Planaria,  as 
described  by  Pearl  (1903),  a  dependence  of  the  reaction  of  the  organism 
on  its  physiological  condition  similar  to  that  which  we  saw  above  for 
Stentor.  The  flatworm  may  be  considered  typical  of  the  lower  bilat- 
eral Metazoa,  so  that  it  will  be  worth  while  to  subject  some  features 
in  its  behavior  to  a  brief  analysis  from  our  present  point  of  view. 

We  may  examine  for  a  simple  typical  case  the  reactions  to  mechani- 
cal stimuli  applied  to  one  side  of  the  anterior  part  of  the  body.  The 
flatworm  is  touched  on  one  side  with  the  tip  of  a  hair  or  of  a  fine  glass 
rod.  The  resulting  response  is  one  of  two  reactions — the  worm  turns 
either  toward  the  point  stimulated  (positive  reaction)  or  away  from  it 
(negative  reaction).  Typically,  the  positive  reaction  is  given  to  a 
weak  stimulus,  while  the  negative  reaction  results  from  a  strong 
stimulus.  The  words  "  weak"  and  "  strong"  have,  as  we  shall  see, 
only  a  relative  meaning  when  used  in  this  connection. 

When,  now,  we  ask  which  of  these  reactions  shall  be  given  as  a 
response  to  a  certain  stimulus,  we  find  that  this  depends  upon  the 
physiological  condition  of  the  organism.  Pearl  finds  the  reactions 
determined  by  the  following  definitely  marked  physiological  states : 

1.  Individuals  are  frequently  in  what  may  be  called  a  resting  con- 
dition.  The  tonus  is  lowered  ;  the  animals  are  very  inactive  and  do 
not  respond  readily  to  stimuli.  This  condition  is  compared  by  Pearl 
with  that  of  sleep  in  higher  animals.  When  a  flatworm  in  this  con- 
dition is  given  a  light  stimulus,  such  as  would  in  an  active  specimen 
induce  a  positive  reaction,  it  does  not  respond  at  all.  If  the  strength 
of  the  stimulus  is  increased,  the  animal  finally  responds  with  a  negative 
reaction,  turning  away  from  the  point  stimulated.  We  may  call  this 
the  condition  of  lowered  tonus. 

2.  In  the  more  usual  active  condition  the  flatworm  gives  the  positive 
reaction  to  a  very  light  touch,  a  negative  reaction  to  a  stronger  stimulus. 
We  may  call  this  the  normal  condition. 

3.  After  the  animal  has  been  repeatedly  stimulated  it  seems  to  become 
excited;  it  moves  about  rapidly,  and  now  gives  always  the  negative 
reaction  to  any  mechanical  stimulus  to  which  it  reacts  at  all.  It  behaves 
much  as  many  higher  animals  do  under  the  influence  of  fear.  We  may 
call  this  the  excited  condition. 


1X6  THB    BEHAVIOR    OF    LOWER    ORGANISMS. 

4.  After  the  worm  in  the  excited  condition  has  been  stimulated 
repeatedly  on  one  side,  so  that  it  turns  its  head  steadily  in  the  opposite 
direction,  after  a  time  it  suddenly  changes  its  method  of  reaction.  It 
jerks  backward,  then  turns  the  anterior  end  quickly  through  a  consider- 
able arc,  usually  toward  the  side  from  which  the  stimulus  is  coming, 
so  that  the  head  now  points  in  an  entirely  new  direction.  Since  the 
stimulus  and  other  external  conditions  remain  the  same,  the  organism 
must  have  passed  into  a  new  physiological  condition,  or  it  would  not 
now  react  in  a  different  way.  We  may  call  this  for  convenience  the 
condition  of  over-stimulation. 

5.  Sometimes  individuals  are  found  which  for  a  brief  period  (two  or 
three  hours)  seem  in  a  much  more  active  condition  than  usual.  They 
move  about  rapidly,  but  do  not  conduct  themselves  like  the  excited 
individuals.  As  they  move  they  keep  the  anterior  end  raised  and  wave 
it  continually  from  side  to  side  as  if  searching.  Specimens  in  this  con- 
dition react  to  almost  all  mechanical  stimuli,  whether  weak  or  strong, 
by  the  positive  reaction,  turning  toward  the  point  stimulated.  Experi- 
mentation failed  to  show  that  this  condition  was  due  to  hunger.  We 
may  speak  of  this  fifth  physiological  condition  as  the  state  of  heightened 
activity. 

In  addition  to  the  effect  of  these  five  well-defined  physiological  states 
on  the  method  of  reaction  to  mechanical  stimuli  at  the  anterior  part  of 
the  body.  Pearl  finds  that  other  less  easily  definable  internal  conditions 
affect  the  reactions.  At  times  an  individual  will  give  the  positive  reac- 
tion to  a  stimulus  of  a  certain  strength  a  few  times,  then  cease  to  give 
it.  On  account  of  these  and  other  complications  due  to  varying  internal 
conditions.  Pearl  concludes : 

It  is  almost  an  absolute  necessity  that  one  should  become  familiar,  or  perhaps 
better,  intimate,  with  an  organism,  so  that  he  knows  it  in  something  the  same 
way  that  he  knows  a  person,  before  he  can  get  even  an  approximation  of  the 
truth  regarding  its  behavior. 

We  have  taken  up  above  only  the  physiological  conditions  influ- 
encing the  reactions  to  simple  mechanical  stimuli  in  the  anterior  region 
of  the  body.  We  find  the  condition  of  affairs  even  here  somewhat 
involved.  When  other  more  complex  stimuli  are  taken  into  considera- 
tion the  results  of  the  interplay  of  change  of  physiological  condition 
and  variations  in  the  stimuli  become,  of  course,  much  more  complicated. 

Thus  we  find  in  the  bilateral  metazoan  Planaria,  as  in  the  unsymmet- 
rical  protozoan  Stentor,  that  we  can  by  no  means  predict  the  behavior 
of  the  individual  from  a  knowledge  of  the  anatomical  structure  and  of 
the  strength  of  the  stimulus.  The  anatomical  structure  limits  the  possi- 
bilities of  reaction  to  several  methods,  which  are,  however,  entirely 
different  or  opposite  in  their  effects  on  the  relation  of  the  organism  to 


PHYSIOLOGICAL    STATES    AS    DETERMINING    JtACTOIIS.  II 7 

the  stimulus.  Just  which  of  these  reactions  shall  be  given  as  a  response 
to  any  particular  stimulus  depends  on  the  physiological  condition  of 
the  organism.  This  physiological  condition  depends  largely,  as  we 
shall  note  later,  on  the  history  of  the  individual.  Thus  no  single  fixed 
schema,  such  as  we  have  in  the  tropism  theory,  can  ever  possibly 
explain  or  define  the  essential  points  in  the  behavior  of  an  animal. 

Stentor  and  Planaria  may  be  taken  as  typical  examples  of  the  higher 
Protozoa  and  of  the  lower  Metazoa,  respectively.  It  is  true  that  we  are 
not  so  well  informed  as  to  changes  in  physiological  condition  in  other 
lower  organisms  as  in  these  two  cases,  but  this  is  unquestionably  due 
merely  to  the  fact  that  investigation  has  not  been  directed  especially  to 
this  point.  There  are,  however,  many  cases  in  the  literature  which 
explicitly  or  implicitly  show  the  importance  of  physiological  conditions 
in  determining  the  behavior  of  lower  organisms.  A  number  of  these 
cases  may  be  brought  together  here. 

CHANGES  IN  THE  SENSE  OF  "  TROPISMS  "  AND  OTHER 
REACTIONS. 

Loeb  (1S93)  and  Nagel  (1894)  have  called  attention  to  the  fact  that 
certain  worms  and  mollusks  respond  to  a  shadow  by  suddenly  with- 
drawing into  their  tubes,  but  that  after  the  first  reaction  has  been  thus 
produced  the  worms  may  no  longer  react.  In  this  "  after  effect  of  the 
stimulus"  (Loeb)  we  have,  of  course,  a  case  of  changed  physiological 
condition. 

Changes  in  the  sense  of  "tropisms"  belong  here.  Groom  &  Loeb 
(1890)  found  that  larvae  of  Balanus  are  at  certain  times  of  the  day 
positively  phototactic  ;  at  other  times  negatively  phototactic.  This 
difference,  in  so  far  as  it  is  independent  of  changed  external  conditions, 
is,  of  course,  due  to  differences  in  the  physiological  condition  of  the 
organism.  Loeb  (1893)  found  that  the  larvae  of  the  moth  Porthesia 
are  positively  phototactic  when  hungry  ;  not  so  after  eating.  Here  we 
have  a  well-defined  physiological  condition  determining  the  nature  of 
the  reaction ;  hunger  is  one  of  the  most  important  conditions  in  many 
of  the  lower  animals.  Sosnowski  (1899)  and  Moore  (1903)  show  that 
the  geotropism  of  Paramecium  changes  from  negative  to  positive  under 
various  conditions.  Towle  (1900)  and  Yerkes  (1900)  have  shown  that 
the  sense  of  the  phototactic  reaction  in  Entomostraca  is  dependent  on 
the  preceding  treatment  of  the  organism,  mere  transference  with  the 
pipette  often  changing  the  sense  of  the  reaction  from  positive  to  nega- 
tive or  vice  versa.  Such  instances  could  doubtless  be  multiplied 
indefinitely.  Each  case  taken  by  itself  seems  perhaps  of  comparatively 
little  significance.  We  may  look  upon  them,  however,  as  indications  of 
an  extensive  dependence  of  behavior  on  physiological  conditions,  such 


IlS  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

as  we  found  in  Stentor  and  the  flatworm.  Thorough  investigation  of 
any  of  these  organisms  from  this  point  of  view  would  doubtless  bring 
to  light  a  variety  of  physiological  conditions  on  which  the  reactions 
depend. 

CHANGES  IN  THE  SENSE  OF  REACTIONS  WITH  CHANGES 
IN  THE  INTENSITY  OF  THE  STIMULUS. 

Must  we  not  bring  under  the  same  point  of  view  the  well-known 
phenomenon  of  a  change  in  the  sense  of  the  reaction  with  a  change  in 
the  intensity  of  the  stimulus  ?  As  a  simplest  case  of  this  we  may  take  the 
reaction  of  Stentor  to  mechanical  stimuli.  As  shown  in  the  ninth  of 
my  studies  (Jennings,  1902),  Stentor  reacts  to  a  very  weak  mechani- 
cal stimulus  on  one  side  of  the  disk  by  bending  toward  the  source  of 
stimulus ;  to  a  stronger  but  otherwise  similar  stimulus  it  responds  by 
contracting  into  the  tube,  or  (later)  by  bending  in  another  direction. 
In  the  same  way  the  flatworm  reacts  positively  to  a  weak  mechanical 
or  chemical  stimulus,  negatively  to  a  stronger  one.  How  can  we  ex- 
plain these  opposite  reactions  to  stimuli  of  the  same  quality,  differing 
only  in  intensity.^ 

We  have  here,  it  seems  to  me,  the  same  phenomenon  shown  in  the 
production  of  a  change  in  physiological  condition  by  a  stimulus.  We 
know  that  even  a  single  stimulus  may  produce  a  changed  physiological 
condition,  as  when  after  a  single  stimulus  the  organism  no  longer 
reacts  as  before.  We  know  also  that  the  nature  of  the  physiological 
condition  determines  the  reaction.  In  the  present  case  we  must  con- 
clude that  a  light  stimulus  throws  the  organism  into  a  certain  physio- 
logical condition,  whose  concomitant  reaction  is  turning  toward  the 
point  stimulated.  A  more  intense  stimulus  induces  a  different 
physiological  condition,  whose  concomitant  reaction  is  a  contraction 
into  the  tube  (Stentor),  or  a  turning  in  the  opposite  direction  (flatworm). 
The  action  of  the  stimulus,  as  we  have  seen  in  the  foregoing  paper 
devoted  to  the  theory  of  tropisms,  cannot  in  most  cases  be  directly  on 
the  motor  organs,  so  that  from  this  point  of  view  also  we  are  almost 
forced  to  the  conclusion  that  the  primary  action  of  the  stimulus  is 
to  change  the  physiological  condition  of  the  organism.  In  any  reac- 
tion to  stimulus  we  would  have,  therefore,  the  following  steps :  The 
stimulus  acting  on  the  organism  changes  its  physiological  condition  ; 
this  physiological  condition  induces  a  certain  type  of  reaction.  In 
determining  what  physiological  condition  shall  be  produced,  the  inten- 
sity of  the  stimulus  is  fully  as  important  as  its  quality. 

We  have  a  similar  reversal  of  the  reaction  as  the  intensity  changes 
in  reactions  to  light.  Many  organisms  are  positive  to  weak  light; 
negative  to  strong  light.      The  cause  of  this  reversal  of  the  reaction  as 


i»MYSIOLOGICAL   STATES   AS    DETERMINII^G    FACTOkS.  119 

the  light  grows  stronger  has  given  rise  to  muph  discussion  (see 
Hoh-nes,  1901  and  1903).  We  have  here,  of  course,  a  parallel  case  to 
the  reversal  of  the  reaction  in  Stentor  or  the  flatworm  under  mechani- 
cal stimuli  of  varying  intensity.  In  the  weak  light  we  must  suppose 
the  organism  to  be  thrown  into  a  certain  physiological  condition,  the 
concomitant  of  which  is  a  certain  type  of  reaction.  In  a  more  intense 
light  a  different  physiological  condition  is  induced,  corresponding  to  a 
different  reaction.  The  fact  that  different  intensities  of  stimuli  do 
cause  different  physiological  conditions  and  different  reactions  is,  of 
course,  familiar  to  us,  both  from  experimentation  on  animals  and  from 
our  own  experience ;  in  the  latter  case  we  usually  call  the  distinctive 
reactions  to  very  intense  stimuli  pain  reactions.  In  the  reversal  of  the 
reaction  to  light  as  the  light  becomes  stronger  we  have,  it  seems  to  me, 
merely  an  instance  of  this  general  phenomenon,  not  differing  in  funda- 
mental character  from  other  instances. 

In  most  of  these  cases  we  have,  of  course,  a  further  problem  in  regard 
to  those  features  of  the  reaction  which  concern  direction.  Why  does 
the  weak  stimulus  on  the  left  side  of  Planaria  cause  a  turning  toward 
that  particular  side?  Or,  why  does  a  weak  light  from  a  certain  direc- 
tion cause  Volvox  to  swim  in  that  particular  direction  ?  These  problems 
of  direction  are,  of  course,  not  touched  in  the  foregoing  discussion, 
which,  however,  loses  none  of  its  force  because  these  problems  remain. 
They  are  simply  farther  problems.  The  tropism  theory  gave  a  simple, 
direct  answer  to  these  questions ;  but,  as  we  have  alreadv  shown  in 
the  foregoing  paper,  this  answer  was,  in  many  cases  at  least,  not  a 
correct  one.  Possibly  some  combination  of  certain  features  of  the 
tropism  theory  with  a  consideration  of  the  facts  of  changes  in  physio- 
logical condition  may  give  us  a  satisfactory  answer  to  the  problems 
of  direction. 

INTERFERENCE  OF  STIMULI. 

Again,  we  have  in  the  interaction  or  interference  of  stimuli  certain 
phenomena  which  seem  to  fall  under  our  present  point  of  view.  First, 
we  have  the  so-called  cases  of  "  heterogeneous  induction,"  where  the 
action  of  one  stimulus  reverses  or  modifies  the  reaction  to  another. 
For  example,  many  cases  are  known  in  which  animals  positively  photo- 
tactic  become  negative,  or  vice  versa^  when  the  temperature  is  changed. 
(For  a  collection  of  such  cases  see  Loeb,  1893,  and  Davenport,  1897, 
p.  199.)  In  these  cases  the  physiological  condition  of  the  organism 
seems  altered  by  one  stimulus  (as  heat  or  cold),  in  such  a  way  that  it 
no  longer  reacts  to  another  stimulus  (light)  as  it  did  before.  In  the 
ciliate  infusoria,  specimens  which  are  in  contact  with  solids  do  not 
react  at  all  to  many  agents  which  under  other  circumstances  call 
forth  a  marked  reaction.     Putter  (1900)  has  made  a  special  study  of 


I20  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

this  matter,  describing  especially  the  interference  of  contact  with  the 
reaction  to  heat  and  to  electricity.  In  the  second  of  these  contributions 
(p.  32),  we  have  seen  that  attached  Stentors  do  not  react  at  all  to 
light.  Physically  considered,  there  is  no  necessary  opposition  between 
the  action  of  contact  and  the  action  of  the  other  stimuli  named.  We 
must  conclude  then  that  contact  with  solids  so  alters  the  physiological 
condition  of  the  organism  that  it  no  longer  reacts  to  the  other  stimuli. 

SPONTANEOUS  MOVEMENTS. 

Further,  we  find  that  alterations  in  physiological  condition  may  cause 
definite  movements,  which  take  place  without  external  stimulus.  Such 
are  the  movements  which  we  call  spontaneous.  As  an  example  of  this 
we  may  take  the  case  of  Hydra.  If  an  undisturbed  green  Hydra  is 
observed  continuously,  it  is  found  to  contract  and  again  to  extend  with- 
out visible  cause  every  i  J  to  2  minutes.  Thus,  it  remains  at  rest  for 
a  period  of,  say,  ij  minutes.  Its  physiological  condition  at  this  time 
we  may  call  X.  At  the  end  of  this  period  it  contracts.  Since  the 
external  conditions  have  not  changed  the  Hydra  itself  niust  have 
changed,  otherwise  it  would  continue  at  rest.  The  physiological  condi- 
tion A^  passes  into  the  condition  T^  and  the  Hydra  as  a  result  contracts. 
This  contraction  is,  of  course,  exactly  the  reaction  given  as  a  response 
to  most  stimuli  in  Hydra.  In  Vorticella  we  find  similar  spontaneous 
contractions  at  intervals,  essentially  as  in  Hydra.  Cases  of  movements 
in  the  lower  organisms  that  are  inaugurated  by  internal  changes  in 
condition  could,  of  course,  be  multiplied  indefinitely.  For  our  present 
point  of  view  it  is  of  importance  to  recognize  clearly  the  fact  that  a 
change  in  physiological  condition  may,  by  itself,  cause  exactly  the  same 
behavior  that  at  other  times  appears  as  a  response  to  external  stimuli. 

METHODS  OF  CAUSING  CHANGES  IN  PHYSIOLOGICAL 
CONDITION. 

Changes  in  physiological  condition  are  thus  evidently  brought  about 
in  a  number  of  different  ways.  We  may  attempt  to  summarize  here 
the  different  methods  which  appear  to  exist  in  the  lower  organisms. 

(i)  A  single  simple  stimulus  may  bring  about  a  change  in  physiologi- 
cal condition.  This  is  proved  by  the  fact  that  the  organism  after  it  has 
received  a  single  stimulus  may  react  differently  from  its  previous 
method.  Thus,  Stentor  reacts  to  a  single  touch,  but  after  this  single 
touch  it  may  no  longer  react  when  touched  in  the  same  way  again ; 
or  it  may  react  in  a  different  manner.  It  is  probable,  further,  that  the 
first  reaction  to  a  single  simple  stimulus  is  to  be  considered  due  to  a 
change  in  physiological  condition  produced  by  this  stimulus. 

(2)  Repetition  of  the  same  stimulus  may  cause  a  change  in  physio- 
logical condition  such  as  is  not  produced  by  a  single  stimulus.     This 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  121 

again  may  be  illustrated  from  the  experiments  on  Stentor,  described 
above  (p.  112). 

(3)  Internal  causes,  not  definable,  may  give  rise  to  changes  in  physio- 
logical condition.  The  result  is  spontaneous  movement  at  intervals, 
as  described  above  for  Vorticella  and  Hydra.  As  many  authors  have 
pointed  out,  rhythmical  SDontaneous  movements  may  be  due  to  a  steady, 
non-rhythmical,  internal  change  of  condition. 

(4)  The  movement  or  reaction  performed  by  the  organism  may 
change  the  physiological  condition.  This  is  illustrated  in  one  way  by 
the  fact  that  after  a  single  spontaneous  contraction  in  Vorticella  or 
Hydra,  the  animal  remains  quiet  for  an  interval,  showing  that  the 
original  physiological  condition  was  restored  by  the  movement.  The 
fact  that  the  reaction  performed  by  the  organism  changes  the  physio- 
logical condition  of  the  latter  is,  of  course,  the  basis  of  the  formation  of 
habits  in  higher  organisms ;  in  this  case  the  performance  of  a  reaction 
once  or  repeatedly  throws  the  organism  into  a  condition  where  it  is 
more  likely  to  react  in  the  same  way  again.  This  particular  method 
of  alteration  of  condition  has  perhaps  not  been  clearly  demonstrated 
for  unicellular  organisms,  though  there  is  some  indication  of  it  in  the 
behavior  of  Vorticella,  as  described  by  Hodge  &  Aikins  (1895),  and 
of  Stentor  as  described  by  myself  in  the  ninth  of  my  studies.  Thus, 
Stentor  responds  to  carmine  in  the  water  by  a  series  of  different  reac- 
tions, finally  reaching  the  condition  where  it  reacts  by  contracting  at 
once  into  its  tube.  If  the  stimulus  is  now  repeated  every  time  the 
Stentor  extends,  it  never  gives  its  earlier  method  of  reaction,  but  reacts 
steadily  for  a  long  time  by  contracting  at  each  stimulus.  Is  this  persist- 
ence in  the  contraction  reaction  due  partly  to  the  fact  that  it  has  begun 
on  this  reaction  method,  and  therefore  keeps  it  up,  or  is  it  due  only  to 
the  fact  that  the  stimulus  has  been  repeated  many  times  ?  In  the  former 
case  the  behavior  would  perhaps  fall  under  our  present  point  of  view ; 
in  the  latter  it  would  not.  Cases  among  the  Protozoa  where  the  repeated 
performance  of  a  reaction  clearly  makes  the  further  performance  of  the 
same  reaction  easier  or  more  likely  to  occur,  would  be  of  much  interest. 

NATURE  OF  REACTIONS  TO  STIMULI. 

The  foregoing  considerations  evidently  have  a  definite  bearing  on 
the  problem  of  the  nature  of  reactions  to  stimuli.  They  lead,  as  set 
forth  briefly  on  page  iiS,  to  the  following  conception  of  the  steps  oc- 
curring in  a  reaction  to  a  stimulus:  (i)  The  stimulus  acting  on  the 
organism  causes  a  change  in  its  physiological  condition ;  (2)  this 
change  in  physiological  condition  gives  rise  to  the  typical  reaction. 

The  evidence  for  this  view  is  found  scattered  throughout  the  fore- 
going discussion  ;  its  main  points  may  be  briefly  summarized  here  as 
follows : 


t%±  THE    SKHAVIOft    OP   LOWER    ORGANISAtS. 

(i)  We  have  seen  that  stimuli  do  unquestionably  cause  changes  in 
physiological  condition.  This  is  demonstrated  by  the  fact  that  after  a 
stimulus  has  occurred  and  ceased  to  act,  the  organism  reacts  differently 
to  the  same  or  other  stimuli.    (For  examples  see  pages  112,  117.) 

(2)  We  have  seen  that  the  changes  in  physiological  condition  do  un- 
questionably cause  definite  movements,  of  exactly  the  sort  that  we  are 
accustomed  to  call  reactions  to  stimuli.  (Contraction  of  Hydra  or  Vor- 
ticella,  etc. ;  see  p.  120.) 

These  two  facts  give  a  solid  foundation  for  the  above  view  of 
reactions  to  stimuli,  and,  indeed,  it  seems  to  me,  raise  a  presumption 
that  reactions  to  stimuli  are,  as  a  rule,  brought  about  in  the  way 
described.     Further  evidence  in  favor  of  this  view  is  as  follows  : 

(3)  In  the  paper  which  precedes  the  present  one  we  have  demon- 
strated that,  in  the  Infusoria  and  Rotifera  at  least,  the  action  of  stimuli 
is  not  directly  on  the  motor  organs  of  that  part  of  the  body  on  which 
the  stimulus  impinges.  The  organism  reacts  as  a  whole,  and  in  a  way 
that  is  not  explicable  even  on  the  assumption  of  a  definite  plan  of  ner- 
vous interconnection  between  the  regions  stimulated  and  the  motor 
organs,  an  assumption  that  is,  of  course,  in  any  case  not  allowable  for  the 
Infusoria.  Such  reactions  cannot  be  explained  otherwise  than  as  due 
to  changes  in  the  physiological  condition  of  the  organism  as  a  whole. 
Further,  evidence  was  given  to  show  that  the  reactions  of  higher  organ- 
isms are  in  many  cases  equally  inexplicable  as  a  result  of  direct  action 
of  the  stimulus  on  the  motor  organs. 

Only  in  the  reaction  of  some  organisms  to  the  constant  electric  cur- 
rent did  we  find  such  conditions  fulfilled  as  permit  an  explanation  of  a 
part  of  the  phenomena  on  the  theory  of  the  direct  action  of  the  agent 
on  that  part  of  the  body  on  which  it  impinges,  in  accordance  with  the 
theory  of  tropisms.  Other  features  of  the  reaction  to  this  stimulus  (in 
many  cases  the  determining  ones)  are  only  explicable  on  the  theory 
that  they  are  due  to  the  physiological  state  of  the  organisms  as  a 
whole,  induced  by  the  stimulus  (see  p.  100).  This  shows  that  we  may 
find  at  any  time  these  two  methods  of  action  mixed,  or  perhaps  eithei 
one  separately.  But  the  reaction  to  the  electric  current  is  the  only  one 
out  of  the  reactions  to  a  multitude  of  agents,  that,  in  the  Infusoria,  has 
been  shown  to  have  this  additional  feature — reactions  of  different  parts 
of  the  body  in  opposed  ways.  The  reaction  to  the  electric  current  is 
thus  of  the  very  greatest  interest,  not  because  it  stands  as  type  for 
reactions  in  general,  but  for  exactly  the  opposite  reason,  because  it 
presents  factors  which  are  not  known  to  occur  in  other  reactions. 

(4)  The  view  that  reactions  to  stimuli  take  place  through  the  inter- 
mediation of  changes  in  the  physiological  condition  of  the  organism  as 
a  whole  is  further  reinforced  by  the  fact,  set  forth  above,  that  it  is  only 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  1 23 

on  the  basis  of  such  a  view  that  we  can  understand  the  changes  of 
reaction  which  occur  when  the  same  stimulus  is  repeated ;  by  the  facts 
of  the  interference  of  stimuli,  even  when  their  direct  physical  action  is 
by  no  means  opposed  ;  by  the  facts  of  heterogeneous  induction,  and  by 
the  fact  that  organisms  at  different  times  of  the  day  or  at  different  sea- 
sons show  different  methods  of  reaction  to  the  same  stimuli. 

(5)  This  view  is  also  strengthened  by  the  fact  that  it  brings  into 
relation  reactions  to  stimuli  and  spontaneous  movements.  On  this  view 
both  are  due  directly  to  the  same  cause,  to  changes  in  physiological 
condition,  produced  in  one  case  by  internal  causes,  in  the  other  by 
external  causes. 

(6)  This  view  receives  powerful  support,  it  seems  to  me,  in  our 
knowledge  of  what  takes  place  in  the  higher  animals,  including  man. 
This  point  I  shall  attempt  to  develop  farther  on  in  the  present  paper. 

This  view,  that  reactions  to  stimuli  in  the  lower  organisms  are  pro- 
duced in  general  through  changes  in  physiological  condition,  is  not,  of 
course,  set  forward  as  anything  new  or  original.  Many  others  have 
doubtless  taken  this  point  of  view,  and  it  is  implied,  perhaps  not  always 
consciously,  in  many  attempted  explanations  of  animal  behavior. 
The  writer  is  merely  attempting  to  emphasize  that  particular  interpre- 
tation, out  of  many  existing  ones,  towards  which  the  facts  seem  to 
point  strongly.  He  is  convinced  that  the  factor  of  physiological  con- 
dition as  determining  behavior  has  not  oeen  so  fully  and  explicitly 
realized  and  dealt  with  in  work  on  the  lower  organisms  as  the  facts 
demand,  and  that  many  things  that  seem  anomalous  fall  into  their 
proper  places  when  this  factor  is  taken  fully  into  consideration. 

What  is  the  nature  of  physiological  conditions,  or  changes  in  phys- 
iological condition  ?  Of  course,  we  are  not  able  to  answer  this  ques- 
tion. One  is  tempted  to  think  of  these  expressions  as  signifying 
something  like  chemical  states  or  changes  in  chemical  states.  But  the 
concept  of  physiological  states  is,  for  higher  animals  at  least,  one  at 
which  we  arrive  by  analysis  of  complex  phenomena  in  behavior,  and 
this  does  not  give  us  any  direct  evidence  as  to  the  real  nature  of  the 
change  in  the  living  substance  (considered  as  matter)  which  takes 
place  when  the  physiological  condition  changes. 

The  concept  ''  physiological  states"  is  a  preliminary  collective  con- 
cept, which  may  later  be  analyzed  into  many.  Such  analysis  is  certain, 
however,  to  be  difficult  and  hypothetical  in  character  in  the  lowest 
organisms.  In  man  we  have,  of  course,  a  basis  for  analysis  in  the  sub- 
jective accompaniments  of  physiological  (here  called  psychological) 
conditions, — in  the  feelings,  emotions,  etc. 


124  "^"^    BEHAVIOR    OF    LOWER    ORGANISMS. 

PHYSIOLOGICAL    STATES   IN  BEHAVIOR  OF  HIGHER  ANIMALS, 
AS  COMPARED  WITH  THOSE  IN  LOWER  ORGANISMS. 

Realization  of  the  fact  that  the  behavior,  even  in  the  lowest  organisms, 
is  determined  to  a  large  degree  by  physiological  states  must  be  of  great 
service  in  welding  into  one  connected  whole  the  study  of  behavior  in 
all  animals,  from  the  lowest  up  to  man.  The  attempt  to  divorce  the 
study  of  the  behavior  of  man  from  that  of  the  lower  animals,  which 
has  been  evident  in  late  years,  seems  unfortunate  and  unnecessary.  It 
is  true  that  we  are  not  justified  in  reading  the  subjective  states  of  man 
directly  into  the  lower  organisms.  But  we  are  not  confronted  with  the 
alternative  of  doing  this  or  of  separating  the  two  subjects  completely. 
The  behavior  of  man  can  be  studied  from  the  same  objective  standpoint 
which  we  employ  in  investigating  the  behavior  of  animals.  When  this 
is  done,  there  is  no  reason  for  holding  the  results  on  man  aloof  from 
those  obtained  elsewhere  ;  if  it  is  proper  to  compare  diflerent  organ- 
isms of  any  kind  from  this  point  of  view,  in  order  to  obtain  general 
results,  as  all  investigators  do,  it  is  certainly  proper  to  draw  man  also 
into  the  circle  of  comparison.  The  fact  that  in  man  we  can  know  also 
the  subjective  accompaniments  of  the  different  physiological  states  and 
reactions  is  by  no  means  a  disadvantage  in  this  comparison  ;  it  is  merely 
an  additional  feature,  of  the  highest  possible  interest.  We  can  even, 
it  seems  to  me,  justifiably  call  attention  to  the  relation  between  the 
subjective  states  as  found  in  man  to  certain  general  phenomena  common 
to  man  and  other  organisms.  It  is  only  when  we  proceed  directly  to 
attribute  to  the  lower  animals  the  subjective  states  which  we  know  only 
in  man  (and,  indeed,  only  in  our  own  individual  minds)  that  we  pass 
the  boundary  of  scientific  procedure. 

In  the  higher  animals,  and  especially  in  man,  the  essential  features 
in  behavior  depend  very  largely  on  the  history  of  the  individual ;  in 
other  words,  upon  the  present  physiological  condition  of  the  individual, 
as  determined  by  the  stimuli  it  has  received  and  the  reactions  it  has 
performed.  But  in  this  respect  the  higher  animals  do  not  differ  in 
principle,  but  only  in  degree,  from  the  lower  organisms,  as  we  have  seen 
in  our  analysis  of  the  behavior  of  Stentor.  In  this  unicellular  form 
we  were  forced  to  distinguish  at  least  six  different  physiological  condi- 
tions, determining  in  the  same  individual  different  reactions  to  the  same 
stimuli.  In  the  higher  animals,  and  especially  in  man,  we  can  distin- 
guish, as  might  be  expected,  an  immensely  greater  number  of  such 
conditions  which  induce  difterent  reactions,  but  there  is  no  evident  differ- 
ence in  principle  in  the  two  cases.  Can  we  go  farther  and  make  a  more 
direct  comparison  of  individual  physiological  states  in  the  higher  and 
lower  organisms?  We  find  in  Stentor,  and  again  in  the  flatworm, 
that  after  the  organism  has  been  repeatedly  stimulated  by  an  agent 


PHYSIOLOGICAL   STATES    AS    DETERMINING   FACTORS.  1 25 

which  must  in  the  long  run  be  classed  as  injurious,  it  is  thrown  into  a 
physiological  condition  in  which  its  reactions  become  more  rapid  and 
powerful,  and  of  such  a  nature  as  to  remove  the  organism  from  the 
source  of  stimulus.  We  find  that  in  this  state  the  organism  reacts  to 
any  stimulus  to  which  it  reacts  at  all  by  a  strong  negative  reaction. 
In  higher  animals  we  frequently  find  the  same  condition  of  affairs,  and 
the  animal  is  then  commonly  said  to  be  frightened.  Finally,  we  often 
find  in  man  a  similar  condition,  and  here  we  know  certain  subjective 
accompaniments  of  the  physiological  condition,  the  most  characteris- 
tic of  which  is  perhaps  the  emotion  of  fear.  In  all  these  cases  the 
objective  manifestations  of  the  physiological  condition  are  of  the  same 
character.  Does  the  fact  that  in  man  we  know  something  additional 
about  the  matter,  the  subjective  accompaniments,  constitute  grounds 
for  denying  the  essential  similarity,  from  a  physiological  standpoint, 
of  this  condition  in  man  and  that  in  the  lower  organisms.?  It  seems  to 
me  that  it  does  not ;  in  fact,  all  that  is  maintained  in  making  the  com- 
parison is  that  this  condition  causes  similar  objective  phenomena  and 
is  brought  about  by  similar  conditions.  Further  than  this  our  analysis 
and  comparison  cannot  go. 

Another  class  of  physiological  conditions  which  we  can  distinguish 
almost  all  the  way  through  the  animal  series  is  that  produced  character- 
istically by  intense  stimuli,  as  opposed  to  faint  stimuli.  As  a  rule,  any 
stimulus,  even  if  it  is  one  to  which  the  organisms  respond  usually  by  a 
positive  reaction,  produces,  when  it  becomes  very  intense,  reactions 
whose  general  effect  is  to  remove  the  organisms  from  the  source  of 
stimulation  (negative  reactions).*  This  is  true  in  Amoeba,  where  weak 
mechanical  stimuli  cause  spreading  out  and  movement  toward  the 
source  of  stimulus,  while  strong  mechanical  stimuli  cause  it  to  contract 
and  move  away ;  it  is  true  for  Stentor ;  it  is  true  for  the  stimulus  of 
weak  and  strong  light  in  Euglena  and  Volvox  and  many  other 
organisms ;  it  is  true  for  mechanical  and  chemical  stimuli  in  the  flat- 
worm  ;  it  is  true  in  general  for  higher  animals  and  man.  In  all  these 
cases  the  intense  stimulus  evidently  changes  the  physiological  con- 
dition so  that  the  organism  now  reacts  negatively.  In  man  we  know 
that  this  physiological  condition  is  accompanied  subjectively  by  pain 
or  at  least  discomfort,  and  even  in  higher  animals  such  reactions  are 
usually  spoken  of  as  pain  reactions.  Objectively  considered,  the 
phenomena  are  analogous  throughout  the  animal  series,   so  that  we 


***All  organisms  behave  in  two  great  and  opposite  ways  toward  stimulations; 
they  approach  them  or  they  recede  from  them.  Creatures  which  move  as  a 
whole  move  toward  some  kinds  of  stimulations,  and  recede  from  others.  Crea- 
tures which  are  fixed  in  their  habitat  expand  toward  certain  stimulations,  and 
contract  away  from  others."     Baldwin,  1897,  p.  199. 


ia6  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

may  properly  characterize  the  physiological  condition  which  produces 
the  negative  reaction  to  strong  stimuli,  with  Professor  J.  Mark  Bald- 
win (1897,  p.  43)  as  the  "  physiological  analogue  of  pain."  This,  of 
course,  by  no  means  commits  us  to  the  belief  that  the  organisms  have 
a  sensation  of  pain  ;  concerning  this  we  know  nothing. 

It  thus  seems  to  me  possible  to  trace  some  of  the  physiological  con- 
ditions which  we  know,  from  objective  evidence,  to  exist  in  man  and 
the  higher  animals,  back  to  the  lowest  organisms.  Many  conditions  that 
we  can  clearly  distinguish  in  man  will  doubtless  be  followed  back  to  a 
common  single  condition  in  the  lower  organisms  ;  but  this  is  exactly  what 
we  should  expect.  Differentiation  takes  place  as  we  pass  upward  in 
the  scale,  in  these  matters  as  in  others. 

The  most  interesting  and  important  field  in  which  we  find  the 
behavior  of  higher  organisms  dependent  on  their  previous  history,  and, 
therefore,  on  their  present  condition  as  influenced  by  previous  experi- 
ence, is  in  that  group  of  phenomena  which  we  call  memory,  or  learning 
by  experience.  Memory  has  as  its  basis  the  general  phenomenon  that 
a  stimulus  received  or  a  reaction  performed  leaves  a  trace  on  the 
organism,  or  modifies  its  condition  in  such  a  way  that  it  later  reacts 
differently  to  the  same  stimulus.  This  basis  of  memory  is,  of  course, 
clearly  present  in  Stentor. 

The  analysis  of  the  different  physiological  conditions  found  in  the 
lower  organisms,  the  influences  to  which  they  are  due,  and  the 
reactions  of  these  organisms  as  influenced  by  physiological  conditions 
certainly  forms  a  most  promising  field  for  research,  and  one  as  yet 
almost  untouched. 

SUMMARY. 

The  present  paper  attempts  to  show,  by  an  analysis  of  certain 
phenomena  in  the  behavior  of  lower  organisms,  taking  Stentor  and 
Planaria  as  types,  that  physiological  states  of  the  organism  are  most 
important  determining  factors  in  reactions  and  behavior.  In  these 
organisms,  to  the  same  stimuli,  under  the  same  external  conditions, 
the  same  individuals  react  at  different  limes  in  radically  different  ways, 
showing  the  existence  of  different  physiological  states  of  the  organism, 
which  determine  the  nature  of  the  reactions.  In  a  unicellular  organ- 
ism (Stentor)  we  can  distinguish  at  least  six  different  physiological 
states,  in  each  of  which  the  organism  has  a  different  reaction  method, 
and  corresponding  facts  are  brought  out  for  the  flatworm.  Scattering 
observations  taken  from  works  on  tropisms,  etc.,  are  shown  to  indicate 
that  the  same  state  of  affairs  is  found  in  other  lower  organisms. 

The  conditions  producing  these  different  physiological  states  are 
examined  and  their  importance  for  the  theory  of  behavior  in  the  lower 
organisms  is  brought  out.     The  relations  of  these  facts  to  ''  interference 


PHYSIOLOGICAL    STATES    AS    DETERMINING    FACTORS.  1 27 

of  stimuli,"  ''heterogeneous  induction,"  "spontaneous  movements," 
and  "changes  in  the  sense  of  reactions  with  a  change  of  intensity  in 
the  stimulus,"  are  developed. 

The  view  is  set  forth  that  in  most  of  the  lower  organisms  a  reaction 
to  stimulus  usually  involves  the  following  factors:  (i)  the  stimulus 
changes  the  physiological  state  of  the  organism  as  a  whole ;  (2)  this 
change  in  physiological  state  induces  a  certain  type  of  reaction. 
Evidence  for  this  view  is  summarized. 

Finally,  it  is  pointed  out  that  realization  of  the  importance  of 
physiological  states  as  determining  factors  in  the  behavior  of  the  lower 
organism  is  of  service  in  bringing  the  study  of  these  organisms  into 
relation  with  that  of  higher  animals  and  man.  An  objective  study  of 
the  behavior  of  these  higher  animals  shows  the  prevalence  of  physio- 
logical states  as  determining  factors  in  behavior,  and  in  some  cases,  at 
least,  some  of  these  states  are  closely  analogous  to  what  we  find  even 
in  unicellular  organisms. 


SIXTH    PAPER. 


THE  MOVEMENTS  AND  REACTIONS 
OF  AMCEBA. 


"9  1 


CONTENTS. 


Introduction:  Objects  of  the  Investigation 131 

Description  of  the  Movements  and  Reactions, 132 

The  Movements, 132 

The  Movements  of  Amoeba  as  described  Formation  and  Retraction  of  Pseudopodia  15a 

by  Rhumbler  and  Butschli ;  Agree-  Surface    Currents    in    Formation    of 

ment  with  Currents  in  a  Drop  of  Pseudopodia  in  contact  with  Sub- 


Fluid  Moving  as  a  Result  of  a  Local 

Decrease  in  Surface  Tension 13a 

Currents  in  Amoeba  as  studied  from  above; 


stratum 152 

Formation  of  Free  Pseudopodia 153 

Withdrawal  of  Pseudopodia 156 

Movements  at  Anterior  Edge i6o 

Lack  of  Backward  Currents 134        Movements  of  Posterior  Part  of  Body. ...  165 

Movements  of  Upper  and  Lower  Surfaces  General  View  of  Movements  of  Amceba  in 

Studied   Experimentally;     Rolling  Locomotion 169 

Movement 138        Some  Characteristics  of  the  Substance  of 

A mceia  verrucosa  siTid  Its  Rdsitivcs.  140  Amoeba 173 

Other  Species  of  Amoeba 146  Fluidity 173 

Historical  on  Rolling  Movements  in  Rhumbler's  Ento-ectoplasm  Process  173 

Elasticity  of  Form  in  Amoeba...........  175 

Contractility  in  Ectosarc  of  Amoeba.  177 


Amoeba 148 


Reactions  to  Stimuli 181 

Reactions  to  Mechanical  Stimuli 181        Some  Complex  Activities 193 

Positive  Reaction 181  Activities  connected  with  Food-taking  193 

Negative  Reaction 182  Taking  Food „ 193 

Reaction  to  Chemical  Stimuli 187  Pursuit  of  Food 196 

Reaction  to  Heat 190  Other  Amoeba  as  Food 198 

Reactions  to  Other  Simple  Stimuli 191  Reactions  to  Injuries aoa 

Physical  Theories  and  Physical  Imitations  of  Amoeboid  Movements,        .     204 

Surface  Tension  Theory 204  Experimental    Imitation    of  Movements 

Berthold's  Theory  that  One-sided  Adher-  due  to  Local  Contractions  of  Ectosarc 

ence  to  Substratum  is  the  Cause  of  and  of  the  Roughening  of  Ectosarc  in 

Locomotion 208  Contraction 215 

Experimental  Imitation  of  Locomo-  Direct  or    Indirect  Action   of   External 

tion  in  Amoeba 209  Agents  in  Modifying  Movements 219 

Formation  of  Free  Pseudopodia 214  Direct  or  Indirect  Action  in  Food-taking,  232 

General  Conclusion 225 

Behavior  of  Amoeba  from  Standpoint  of  Comparative  Study  of  Animal 

Behavior, 226 

Habits  in  Amoeba - 226        Relation  of  Different  Reactions  to  Differ- 

Classes  of  Stimuli  to  which  Amoeba  Re-  ent  Stimuli;    Adaptation  in  Beha- 

j^cts 227  vior  of  Amoeba aa; 

Types  of  Reaction 227        Reflexes  and  "Automatic  Actions"   in 

Amoeba 228 

Variability  and  Modifiability  of  Reactions  229 

Summary 230 

130 


THE   MOVEMENTS   AND    REACTIONS    OF  AMCEBA. 


INTRODUCTION:   OBJECTS  OF  THE  INVESTIGATION. 

The  present  paper  contains  the  results  of  an  investigation  which  was 
undertaken  with  two  general  problems  in  mind.  The  first  purpose 
was  to  determine  by  observation  and  experiment,  from  the  standpoint 
of  the  student  of  animal  behavior,  how  far  recent  physical  and 
mechanical  theories  go  in  aiding  us  to  explain  the  behavior  of  Amoeba. 
The  second  object  of  the  work  was  to  furnish  needed  additional  data 
on  the  reactions  of  Amoeba  to  stimuli,  and  to  systematize  and  unify 
our  knowledge  of  its  behavior. 

The  recent  theories  which  would  resolve  the  activities  of  Amoeba 
largely  into  phenomena  due  to  alterations  in  the  surface  tension  of  a 
complex  fluid  seem  to  promise  much.  They  are  of  precisely  the 
character  from  which  most  may  be  hoped  ;  from  a  study  of  the  physics 
of  matter  in  a  state  similar  to  that  found  in  the  living  substance,  the 
laws  of  action  of  this  living  substance  are  sought.  Such  theories  have 
been  developed,  as  is  .well  known,  by  Berthold  (1886),  Quincke 
(1S88),  Biitschli  (1892),  Verworn  (1892),  Rhumbler  (1898),  Bern- 
stein (1900),  Jensen  (1901),  and  others.  The  success  of  this  method 
of  attacking  the  problems  seems  great.  Activities  similar,  at  least 
externally,  to  those  of  Amoeba,  are  produced  by  physical  means,  and 
fully  analyzed  from  the  physical  and  mechanical  standpoint.  In  this 
manner  the  movement,  the  control  of  movement  by  external  agents, 
the  feeding,  the  choice  of  food,  the  making  of  the  shell,  and  other 
features  of  the  behavior  have  been  more  or  less  closely  imitated,*  and 
in  a  way  permitting  a  complete  analysis  in  accordance  with  chemical 
and  physical  laws. 

From  the  standpoint  of  the  student  of  animal  behavior,  the  resolu- 
tion of  the  behavior  of  any  organism  into  the  action  of  known  physical 
laws  must  be  a  matter  of  the  deepest  interest.  The  actions  of  higher 
organisms  seem  at  present  so  far  from  such  a  resolution  that  some 
investigators  believe  an  essential  difierence  in  principle  to  exist 
between  the  behavior  of  living  things  and  non-living  things  ;  between 
the  laws  of  biology  and  those  of  physics.  The  resolution,  then,  of  the 
behavior  of  even  the  simplest  organism  into  known  physical  factors 
would  be  an  event  of  capital  significance,  affecting  fundamentally  the 
whole  theory  of  animal  behavior.     A  renewed  thorough  study  of  the 


*  See  especially  Rhumbler,  1898.  131 


132  THE    BEHAVIOR   OF   LOWER   ORGANISMS. 

facts,  with  especial  reference  to  these  theories,  seems,  therefore,  much 
to  be  desired.  The  results  of  the  present  study  will  show,  I  believe, 
that  such  a  re-examination  of  the  facts  was  greatly  needed. 

As  to  the  second  object  of  this  investigation,  stated  above,  it  is  a 
somewhat  remarkable  fact  that  the  observational  basis  for  a  number  of 
the  most  important  reactions  assumed  to  exist  in  Amoeba  is  exceedingly 
scanty,  particularly  so  far  as  control  of  the  direction  of  movement  is 
concerned.  For  example,  one  of  the  reactions  most  often  assumed  to 
exist  in  Amoeba,  and  most  commonly  selected  for  imitation  by 
physical  means,  is  chemotaxis,  the  movement  toward  or  away  from  a 
diffusing  chemical.  But  no  account  exists,  so  far  as  I  have  been  able 
to  discover,  of  actual  observation  of  such  a  reaction  in  Amoeba,  under 
experimental  conditions.  Again,  the  effects  of  slight  or  of  intense 
localized  mechanical  stimuli,  in  controlling  the  direction  of  movement, 
has  not  been  worked  out  in  detail.  To  fill  these  and  similar  gaps  in 
our  knowledge,  and  to  bring  the  different  reactions  into  relation  with 
each  other,  so  as  to  make  possible  a  connected  account  of  the  behavior 
of  Amoeba,  is,  then,  the  second  object  of  this  paper. 

I  shall  first  give  an  account  of  the  movements  and  reactions  of 
Amoeba,  as  determined  by  observation  and  experiment,  without  enter- 
ing in  detail  upon  the  theories  of  the  subject.  This  will  be  followed 
by  a  section  dealing  with  the  physical  theories  and  physical  imitations 
of  the  movements  and  reactions,  in  the  light  of  the  facts  set  forth  in  the 
first  section.  A  brief  final  section  will  be  devoted  to  a  characterization 
of  the  behavior  of  Amoeba  from  the  standpoint  of  the  student  of 
animal  behavior. 

I  am  compelled  to  give  a  full  description  of  the  normal  movements 
of  Amoeba,  as  the  course  of  the  investigation  showed  that  the  prevalent 
conception  of  these  movements,  on  which  many  of  the  theories  have 
been  based,  is  not  correct. 

DESCRIPTION  OF  THE  MOVEMENTS  AND   REACTIONS. 
THE  MOVEMENTS. 

MOVEMENTS  OF  AMCEBA  AS  DESCRIBED  BY  RHUMBLER  AND  BUTSCHLI  ; 
AGREEMENT  WITH  CURRENTS  IN  A  DROP  OF  FLUID  MOVING  AS  A  RE- 
SULT OF  LOCAL  DECREASE  IN  SURFACE  TENSION. 

There  are  few  subjects  that  have  been  studied  more  than  the  nature 
of  the  movements  of  Amoeba,  but  nothing  final  has  been  reached,  even 
from  the  descriptive  standpoint.  The  first  preliminary  to  an  under- 
standing of  the  nature  of  the  movements  must  be  to  determine  just  what 
movements  take  place. 

The  most  extensive  recent  study  of  the  movements  of  Amoeba  has 
been  made  by  Rhumbler  (1898),  though  the  magnificent  monograph  of 


THE    MOVEMENTS    AND    REACTIONS    OF   AMGBBA. 


133 


the  Rhizopods  by  Penard  (1902)  contains  incidentally  a  large  number 
of  valuable  observations  on  this  matter. 

According  to  Rhumbler  (/.  c.)  the  movements  in  normal  locomotion 
are  typically  as  follows  :  From  the  hinder  end  of  the  Amoeba  (or  of  the 
pseudopodium,  if  a  single  pseudopodium  is  under  consideration)  a 
current  of  endosarc  passes  forward  in  the  middle  axis  ;  in  front  this  flows 
outward  toward  the  sides,  then  backward  along  the  surface,  gradually 
coming  to  rest.  Figs.  30  and  31 ,  taken  from  Rhumbler,  give  diagrams 
of  these  currents  in  an  Amoeba  moving  as  a  whole  (Fig.  30),  and  in 
the  formation  of  pseudopodia  (Fig.  31).  In  an  Amoeba  which  forms 
more  than  one  pseudopodium  at  once,  these  typical  currents  become 
somewhat  complicated  (Fig.  32),  but  retain  their  main  features.  The 
backward  current  shown  at  the  sides  in  Figs.  30-32  is  conceived  to  be 
present  also  above  and  below,  that  is,  over  the  whole  surface  of  the 
Amoeba.  A  diagram  of  the  currents  in  side  view,  as  given  by  Rhum- 
bler, is  shown  in  Fig.  33,  B.  An  essentially  similar  account  of  the 
currents  is  given  by  Biitschli  (1880,  1892). 


Fig.  30.* 


Fig.  3i.t 


Fig.  324 


Fig.  33.  § 


The  most  striking  feature  in  the  currents  as  above  set  forth  is  the  fact 
that  they  agree  precisely  with  the  currents  produced  in  a  drop  of  fluid 
of  any  sort  when  the  surface  tension  is  lowered  over  a  certain  limited 
area.  There  is  always  a  current  over  the  surftice  away  from  the  region 
where  the  tension  is  lowered,  while  an  axial  current  moves  toward  the 


*  Fig.  30. — Diagram  of  the  currents  in  a  progressing  Amoeba  Umax,  after 
Rhumbler  (1S98). 

fFiG.  31. — Diagram  of  the  **  fountain  currents  "  in  pseudopodia  of  Amoeba, 
after  Rhumbler  (1898). 

J  Fig.  32. — Diagram  of  complex  '*  (puntain  currents"  in  an  Amoeba  with  two 
large  pseudopodia,  after  Rhumbler  (1898). 

§  Fig.  33. — Comparative  diagrams  of  the  currents  in  a  rolling  movement,  and 
in  the  movement  of  Amoeba,  as  conceived  by  Rhumbler,  viewed  from  the  side. 
In  A  are  represented  what  Rhumbler  conceives  to  be  the  necessary  currents  in 
a  rolling  movement,  while  B  represents  what  Rhumbler  considers  the  really 
existing  currents  in  Amoeba,  as  seen  from  the  side.  The  heavier  arrows  in  each 
case  represent  the  current  on  the  lower  surface.     After  Rhumbler  (1898). 


134  "^^^   BEHAVIOR   OF   LOWER   ORGANISMS. 

point  of  lowered  tension.  Diagrams  of  the  movement  of  such  drops 
are  given  in  Fig.  34.  Further,  the  drop  may  elongate  in  the  direction 
of  the  axial  current,  and  may  move  bodily  in  that  direction,  just  as 
happens  in  Amoeba.*  It  is  most  natural,  therefore,  to  conclude  as 
Biitschli  (1892)  and  Rhumbler  (1898)  have  done,  that  the  movements 
of  Amoeba  are  likewise  due  to  a  lowering  of  the  surface  tension  at  the 
anterior  end,  provided  that  its  movements  really  take  place  in  the 
way  described  above, 

CURRENTS  IN  AMCEBA  AS  STUDIED  FROM  ABOVE  ;  LACK  OF  BACKWARD 

CURRENTS. 

At  the  beginning  of  my  work  I  had  no  doubt  that  the  movements 

occurred  exactly  as  above   described,  and,  therefore,  did   not  devote 

special  attention  to  this  point.      But  I  was  soon  struck  by  the  fact  that 

I  was  unable  to  see  any  backward  current  at  the  sides,  as  represented 

in  Figs.   30  and  31.     Further   careful    study    of  the    movements   of 

Amoeba  limax^  A.  proteus^  A.  angulata^  A.  verrucosa^  A.  sphcero- 

nucleolus^  and  one  or  two 

undetermined  species 

confirmed  this  fact,  and  I 

may  say  at  once  that  after 

several  months'  continu- 

^  T^  J.  ous  study  of  the    move- 

FiG.34.t  ^  A  .'  c 

ments    and    reactions  of 

Amoeba  I  have  never,  except  in  one  or  two  doubtful  instances,  seen 
any  backward  movement  of  the  substance  at  the  sides  or  on  the  surface 
of  an  Amoeba  that  was  moving  forward  in  a  definite  direction. 

It  is  true  that  in  the  movements  of  Amoeba  Umax,  for  example,  one 
receives  the  impression  of  two  sets  of  currents,  one  forward  in  the  cen- 
tral axis,  the  other  backward  at  the  sides.  But  if  the  latter  is  studied 
carefully  it  is  found  that  there  is  really  no  current  here ;  the  proto- 
plasm is  at  rest,  and  the  impression  of  a  backward  current  at  the  sides 
is  produced  only  by  contrast  with  the  forward  axial  current.     Amoeba 


*  All  these  facts  are  easily  verified  by  placing  a  drop  of  clove  oil  on  a  slide  in 
a  mixture  of  two  parts  glycerine  to  one  part  95  per  cent  alcohol  under  a  cover 
supported  by  glass  rods,  as  described  in  a  previous  paper  by  the  present  author 
(Jennings,  1902).  By  mixing  some  soot  or  India  ink  with  the  clove  oil  the  cur- 
rents are  made  evident. 

t  Fig.  34. — Currents  in  a  drop  of  fluid  when  the  surface  tension  is  decreased 
on  one  side.  A,  the  currents  in  a  suspended  drop,  when  the  surface  tension  is 
decreased  at  a.  After  Berthold  (1886).  B,  axial  and  surface  currents  in  a  drop 
of  clove  oil,  in  which  the  surface  tension  is  decreased  at  the  side  a.  The  drop 
elongates  and  moves  in  the  direction  of  a,  so  that  an  anterior  (a)  and  a  posterior 
{p)  end  are  distinguishable. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  1 35 

Umax  contains  usually  a  large  number  of  fine  granules,  which  in  many 
cases  extend  to  the  very  outer  surface,  so  that  it  is  not  possible  to  dis- 
tinguish an  ectosarc,  in  the  sense  of  a  layer  containing  no  granules. 
By  watching  the  movements  of  these  particles  it  is  possible  to  determine 
the  direction  of  the  currents  in  the  protoplasm.  The  movements  in 
locomotion  are  usually  as  follows ;  At  the  anterior  end  there  pushes 
forth  from  the  interior  a  clear  substance,  which  I  will  call  the 
hyaloplasm.  As  this  moves  forward  it  spreads  out  laterally,  till  it 
reaches  a  position  such  that  it  forms  a  continuation  forward  of  the 
remainder  of  the  lateral  boundary  of  the  animal.  Into  this  hyaloplasm 
flows  then  the  granular  endosarc.  The  granules  flow  forward,  rapidly 
in  the  middle,  usually  more  slowly  near  the  sides.  As  it  reaches  the 
anterior  end  the  central  current  spreads  out  in  a  fanlike  manner,  so 
that  some  of  the  granules  approach  closely  the  lateral  borders  of  the 
Amoeba  (Fig.  35).  They  then  stop,  while  the  central  part  of  the  cur- 
rent passes  on,  following  the  advancing  anterior  end. 

So  long  as  one  confines  his  attention  to  the  Amoeba  alone,  not 
observing  external  objects, 
one  receives  the  impres- 
sion that  there  are  two 
sets  of  currents,  an  axial 
current  forward,  marginal 

currents  backward.     But 

a         u-  Fig.  35.* 

as  soon  as  one  nxes  his  •'^ 

eye  upon  a  particular  granule  in  the  apparent  backward  marginal 
current,  and  observes  its  relation  to  some  external  object,  he  dis- 
covers that  no  such  current  exists.  The  granule  remains  quiet, 
retaining  continually  its  position  with  relation  both  to  other  granules 
in  the  edge  of  the  Amoeba  and  to  objects  external  to  the  Amoeba. 
Meanwhile  the  remainder  of  the  substance  of  the  Amoeba  is  flowing 
past,  so  that  the  granule  in  question  after  a  time  comes  to  occupy 
a  position  at  the  middle  of  the  length  of  the  Amoeba.  At  about 
this  point  it  usually  begins  to  move  slowly  forward  again,  though 
much  less  rapidly  than  the  internal  current.  The  nature  of  this 
slow  forward  movement  we  shall  take  up  later  (p.  166).  The  main 
portion  of  the  body  of  the  Amoeba  thus  continues  to  pass  the  granule, 
and  the  latter  finally  reaches  the  posterior  end.  Here  it  usually  re- 
mains quiet  for  a  time  (moving  forward  only  as  the  posterior  end  is 
dragged  forward).  Then  it  is  taken  into  the  central  current  again, 
passes  to  the  anterior  end,  and  comes  to  rest  as  before,  while  the 
remainder  of  the  Amoeba  passes  it  by ;  and  this  process  is  repeated 


*  Fig.  35. — Diagram  of  the  movements  of  particles  in  an  advancing  Amoeba. 
Each  broken  line  represents  the  path  of  a  particular  particle. 


136  THE   BKHAVIOIl   OF   LOWER   ORGANISMS. 

indefinitely.  In  favorable  cases  I  have  repeatedly  followed  a  single 
granule  from  the  posterior  end  forward  till  it  came  to  rest  at  the 
anterior  end,  then  watched  the  body  of  the  Amoeba  pass  it  by,  until  it 
was  again  at  the  posterior  end  and  started  forward  anew.  The  course 
of  a  single  granule  is  represented  in  Fig.  36.  As  is  evident  from  this 
figure,  the  granule  does  not  travel  backward  in  any  part  of  its  course. 
Not  all  the  granules,  however,  remain  quiet  until  they  have  passed  to 
the  posterior  end.  Many  of  them  are  taken  again  into  the  central 
stream  before  the  entire  body  of  the  Amoeba  has  passed  them.  Large 
granules  usually  stop  only  a  short  time,  starting  forward  again  before 
the  middle  of  the  Amoeba  has  reached  them  ;  others  are  taken  up  at  the 
middle  or  farther  back,  while  many  smaller  granules  reach  the  posterior 
end.  But  as  a  rule  none  show  any  movement  backward,  so  far  as  I 
have  observed. 

It  is  not  only  at  the  margins  of  the  Amoeba,  but  also  on  the  under 
surface,  in  contact  with  the  substratum,  that  the  ectosarc  with  its 
granules  is  at  rest  or  moving  slowly  forward  in  the  posterior  half. 
This  is  evident  when  the  lower  surface  of  a  transparent  Amoeba  is 
brought  into  focus. 

2  That  excellent  observer, 

/  <^^ __^    Dr.  Wallich,  saw  clearly 

r^ 7^*^^~-— ''''  /^TTin^r-^ )     "^^ny  years  ago  that  there 

V_£^^~~,^v_^ ^Illja^^rrrr^^:^        j      vf     is  really  no  backward  cur- 

O.  g  'c  "^  e        J    rent,  though  at  first  view 

Fig.  36.*  there  appears  to  be  such. 

It  is  only  necessary  to  watch  a  specimen  of  Amoeba  carefully  to  become  con- 
vinced that  the  appearance  of  a  returning,  as  well  as  an  advancing,  stream  of 
granules  is  illusory.  The  stream,  it  will  be  observed,  is  invariably  in  the  direc- 
tion of  the  preponderating  pseudopodial  projections.  The  particles  simply  flow 
along  with  the  advancing  rush  of  protoplasm.  There  is  no  return  stream,  but 
the  semblance  of  one  is  engendered  by  one  layer  of  particles  remaining  at  rest 
whilst  another  is  moving  past  them.    (Wallich,  1863,  ^>  P*  33i-) 

This  statement  of  the  facts  my  observations  fully  confirm. 
In  this  account  of  the  lack  of  backward  movement  in  the  granules 
of  the  ectosarc  on  the  lower  surface  and  at  the  margins  I  find  myself 


*FiG.  36. — Diagram  of  the  movements  of  a  single  particle  in  Amoeba,  as 
seen  from  above.  The  particle  begins  at  a,  passes  to  b  and  then  to  c,  at  the 
anterior  edge  of  the  Amoeba  shown  in  the  outline  i.  The  Amoeba  now  passes 
forward  to  the  position  2,  and  thence  to  3,  while  the  particle  retains  the  posi- 
tion c;  when  the  Amoeba  has  reached  the  position  3  the  particle  is  thus  at 
its  posterior  end.  Now  the  particle  moves  forward  again,  from  c  to  <f,  and 
thence  to  e  and/",  thus  coming  again  to  the  anterior  edge.  Here  it  stops,  as  at 
c,  until  the  body  of  the  Amoeba  has  passed  it.  As  the  figure  shows,  the  particle 
does  not  move  backward  in  any  part  of  its  course. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I37 

at  variance  with  certain  statements  of  F.  E.  Schulze,  Biitschli,  and 
Rhumbler.  I  am  aware  that  this  conflict  of  my  observations  with 
those  of  the  investigators  named,  who  deservedly  rank  among  the 
highest  in  the  field  at  present  under  consideration  as  well  as  elsewhere, 
renders  the  utmost  caution  necessary  in  trusting  to  these  results.  Yet, 
with  this  consideration  in  mind,  and  with  the  confident  expectation  in 
undertaking  the  work  that  I  should  find  the  currents  exactly  as  described 
by  these  authors,  I  have  been  unable  to  come  to  any  result  save  that 
above  set  forth.  The  statements  of  Schulze  (1875,  pp.  344-348)  deal 
with  Pelomyxa  palustris  Greef.  In  this  animal,  according  to  Schulze, 
there  are  resting  portions  at  the  sides  of  the  body,  while  from  behind 
currents  pass  forward  through  the  channel  enclosed  by  these  resting 
portions.  At  the  anterior  end  the  lateral  parts  of  these  currents  turn 
outward  and,  finally,  a  little  backward ;  any 
given  portion  passes  backward  but  a  short  dis- 
tance. The  currents  are  shown  by  Schulze  in 
a  figure,  a  reduced  copy  of  which  is  given  here- 
with (Fig.  37).  According  to  Schulze  the  cur- 
rents have  this  form  on  the  upper  surface  as  well  l'+^*^'*^^V\\lTui/^//'^  Vr}— :v 
as  at  the  sides — that  is,  a  part  of  the  current  flows 
upward  and  backward  on  the  upper  surface. 
Biitschli  (1892,  Anhang,  p.  220)  confirms  this 
account  of  the  currents  in  Pelomyxa. 

I  regret  that  I  have  been  unable  to  obtain 
specimens  of  Pelomyxa  in  order  to  examine 
these   phenomena   for    myself.      One  would   of 

course  be  bold  to  doubt  the  correctness  of  the 

Fig.  ^7  * 
observations  of  such    investigators    as    Schulze 

and  Biitschli,  and  it  is  possible  that  Pelomyxa  differs  from  Amoeba 
in  this  respect.  Yet,  as  we  shall  see  later  (p.  149),  the  account  given 
by  these  authors  is  certainly  incorrect  so  far  as  the  backward  cur- 
rents on  the  upper  surface  are  concerned  ;  it  is  possible,  then,  that  the 
appearance  of  a  backward  current  elsewhere  was  deceptive. 

Rhumbler  (1898)  describes  the  forward  axial  and  the  backward  side 
currents  in  various  species  of  Amoeba,  and  considers  such  movements 
as  typical,  basing  his  theory  of  locomotion  upon  them.  It  seems 
probable  that  slight  backward  currents,  such  as  were  described  by 
Schulze  (Fig.  37),  do  occur  at  times  at  the  sides  of  the  advancing 
anterior  end.  The  posterior  part  of  the  Amoeba  is  narrow  and 
rounded,  the  anterior  part  broad  and  thin.  The  current  of  endosarc 
flows  from  this  narrow  posterior  portion  into  the  broad  anterior  part 

*FiG.  37.— Currents  in  a  progressing  Pelomyxa,  as  seen  from  above,  after 
Schulze  (1875).     The  longer  arrows  represent  stronger  currents. 


138  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

and  must  therefore  spread  out ;  it  would  not  be  unnatural  for  the 
currents  to  flow  even  backward  a  little,  as  in  Schulze's  figure  (Fig. 
37),  in  order  to  fill  the  area  just  in  front  of  the  resting  portion  of  the 
protoplasm  (at  x,  Fig.  37).  As  we  shall  see,  such  movement  is 
sometimes  to  be  observed  in  inorganic  fluids  under  similar  conditions 
(p.  211).  Whatever  the  explanation  of  the  difference  between  my 
observations  and  those  of  the  investigators  named,  the  point  of  impor- 
tance is  that  the  backward  current  is  not  a  constant  nor  an  essential 
part  of  the  locomotion  of  Amoeba,  so  that  it  does  not  form  a  fitting 
basis  for  a  theory  of  locomotion.  Further,  as  we  shall  see,  I  am  able 
to  demonstrate  conclusively  the  incorrectness  of  that  conception  of  the 
nature  of  amoeboid  movement  for  which  alone  the  account  of  the 
currents  given  by  Biitschli  and  Rhumbler  is  significant. 

It  is  evident  that  the  method  of  movement  here  described  is  better 
adapted  to  the  production  of  locomotion  in  a  given  direction  than  that 
which  Biitschli  and  Rhumbler  describe  (see  Figs.  30-33),  since  accord- 
ing to  their  account  a  portion  of  the  substance  of  the  body  is  first  trans- 
ported forward,  then  backward.  In  the  locomotion  as  I  observed  it 
there  is  no  such  useless  transportation  of  substance  in  a  direction 
opposed  to  that  in  which  the  animal  is  traveling. 

On  the  other  hand,  the  movements  as  I  have  described  them  bear 
much  less  resemblance  to  those  produced  in  drops  of  fluid  by  local 
changes  in  surface  tension  (Fig.  34) .  There  is  only  the  slight  turning 
outward  at  the  anterior  end  that  can  be  at  all  compared  to  the  backward 
flow  of  an  outer  layer  in  the  inorganic  drop.  Rhumbler  himself  notes 
that  in  Amoeba  angulata  there  is  often  no  such  backward  current  to 
be  seen  (Rhumbler,  1898,  p.  120),  but  bases  his  theory  of  the  forward 
movement  entirely  on  the  cases  where  it  (supposedly)  does  occur.  In 
Amoeba  angulata^  A.  verrucosa^  and  A.  sphceronucleolus^  according 
to  my  observations,  there  is  often  no  indication  even  of  the  turning 
out  of  the  particles  in  a  fanlike  manner  ;  they  merely  flow  forward  and 
stop  for  a  time.  Biitschli  (1892,  p.  199)  notes  that  the  backward  cur- 
rent at  the  anterior  end  of  Amoeba,  required  by  the  surface  tension 
theory,  is  very  slight,  but  conceives  it  to  be  sufliicient  to  fulfill  the 
requirements  of  the  theory. 

MOVEMENTS    OF    UPPER    AND    LOWER    SURFACES   STUDIED  EXPERIMEN- 
TALLY  ROLLING  MOVEMENT  IN  AMCEBA. 

Thus  far  we  have  left  out  of  consideration  the  movement  of  substance 
on  the  upper  surface  of  the  Amoeba.  It  is  usually  assumed  that  the 
condition  here  is  the  same  as  at  the  sides  and  on  the  under  surface ; 
thus  Rhumbler  gives  a  diagram,  reproduced  in  my  Fig.  33,  B^  showing 
the  backward  current  of  the  upper  surface.     The  positive  observations 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


139 


on  this  point  are  those  of  Schulze  (1875),  Berthold  (1886,  p.  109),  and 
Biitschli  (1892,  p.  220).  These  authors  all  agree  that  the  backward 
current  visible  at  the  sides  of  the  anterior  end  in  Pelomyxa  are  clearly 
also  present  on  the  upper  surface.  It  is  not  usually  possible  to  observe 
particles  moving  backward  on  the  upper  surface  of  Amoeba,  nor  even 
particles  at  rest,  though  this  might  be  due  to  the  fact  that  the  granules 
have  sunken  downward,  leaving  the  upper  surface  clear.  But  to 
decide  whether  the  currents  in  Amoeba  are  essentially  like  those  pro- 
duced in  a  drop  of  fluid  by  a  local  change  in  surface  tension,  it  is  most 
important  to  determine  with  certainty  what  is  taking  place  on  the  upper 
surface. 

Evidently  the  most  natural  way  of  doing  this  is  to  cause,  if  possible, 
some  small  object  to  rest  upon  or  become  attached  to  the  upper  surface 
of  Amoeba,  then  to  observe  the  movement  of  this  object.  This  can  be 
done  by  mingling  a  considerahjle  quantity  of  soot  with  the  water  in 
which  the  Amoebae  are  found.    Some  of  the  soot  particles  settle  on  the 


Fig.  38.*  Fig.  39. t 

upper  surface  of  the  Amoebae,  and  in  some  species  they  adhere  to  this 
surface. 

I  was  quite  unprepared  for  the  results  of  this  experiment.  The 
upper  surface  of  Amoeba  moves  forward,,  not  backward,  as  required 
by  the  surfiice  tension  theory ;  nor  is  it  at  rest  like  the  lower  surface. 


*  Fig.  38, — Movements  of  a  particle  attached  to  the  outer  surface  of  Amoeba 
verrucosa.  When  first  seen  the  particle  was  at  the  posterior  end  (/) ;  it  then 
moved  forward,  as  shown  by  the  arrows,  until  it  passed  around  the  anterior  end 
{a)  to  the  under  side.  (The  Amoeba  itself  of  course  moved  forward  at  the  same 
time;  no  attempt  is  made  to  represent  its  movement  in  the  figure.) 

t  Fig.  39. — Diagram  of  the  movements  of  a  particle  attached  to  the  outer 
surface  oi  Amoeha  verrucosa^  in  relation  to  the  movements  of  the  animal.  The 
Amoeba  is  seen  from  above.  In  the  position  i  the  particle  is  at  the  anterior  end 
of  tlie  Amoeba.  As  the  Amoeba  moves  forward,  it  passes  over  the  particle, 
which  retains  its  place.  Thus  when  the  Amoeba  has  reached  the  position  2  the 
particle  is  at  the  middle  of  its  lower  surface;  when  it  reaches  3  the  particle  is  at 
its  posterior  end.  The  particle  then  passes  upward  and  forward,  as  shown  by 
the  arrows,  so  that  when  the  Amoeba  reaches  the  position  4  the  particle  is  in 
front  of  the  middle,  on  the  upper  surface. 


140  THE   BEHAVIOR   OF   LOWER    ORGANISMS. 

AMCEBA   VERRUCOSA    AND    ITS    RELATIVES. 

In  giving  an  account  of  the  experiments  w^hich  demonstrate  this,  I 
shall  begin  with  species  of  Amoeba  in  which  pseudopodia  are,  as  a  rule, 
not  formed,  and  the  movements  are  uniform  in  character,  since  here  the 
conditions  are  simplest  from  our  present  standpoint.  For  this  purpose 
Amoeba  verrucosa  Ehr.,  and  particularly  the  transparent  form  known 
as  A.  spkceronucleolus  Greef,  are  favorable.  In  these  Amoebae  particles 
cling  rather  easily  to  the  outer  surface. 

When  a  quantity  of  soot  is  added  to  the  water  containing  Amoebae 
of  the  species  named,  small  masses  cling  to  the  surface  of  the  animal. 
Such  a  mass,  attached  to  the  upper  surface,  shows  the  following 
movements  :  It  passes  slowly  forward  (Fig.  38) ,  then  over  the  anterior 
edge,  and  under  the  latter.  Here  it  stops,  while  the  Amoeba  continues 
to  move  forward.  The  mass  of  soot  remains  quiet  until  the  entire 
Amoeba  has  passed  over  it  and  it  lies  beneath  the  posterior  end.  It 
now  passes  upward  again,  to  the  upper  surface  (Figs.  39,  40),  then 
forward  once  more  to  the  anterior  end.     Here  it  goes  under  the  Amoeba 


Fig.  40.* 

as  before,  to  be  carried  upward  and  forward  again  when  the  posterior 
end  passes  over  it. 

These  observations  are  made  with  absolute  ease,  and  there  is  no  pos- 
sibility of  mistaking  internal  particles  for  external  ones.  Particles  lying 
in  the  water  outside  the  Amoeba  may  be  seen  to  become  attached  at  the 
posterior  end,  to  pass  upward,  lying  distinctly  outside  the  boundary  of 
the  protoplasm  (Fig.  38,  posterior  end),  then  forward,  till  as  they  double 
the  anterior  end  they  are  again  seen  sharply  defined  outside  the  boundary 


♦  Fig.  40. — Diagram  of  the  movements  of  a  particle  attached  to  the  surface  of 
Amoeba  verrucosa,  in  side  view.  In  position  i  the  particle  is  at  the  posterior 
end;  as  the  Amoeba  progresses  it  moves  forward,  as  shown  at  2,  and  when  the 
Amoeba  has  reached  the  position  3  the  particle  is  at  its  anterior  edge,  at  x. 
Here  it  is  rolled  under  and  remains  in  position,  so  that  when  the  Amoeba  has 
reached  the  position  4  the  particle  is  still  at  x,  at  the  middle  of  its  lower  surface. 
In  the  position  5  the  particle  is  still  in  the  same  place,  x,  save  that  it  is  lifted 
upward  a  little  as  the  posterior  end  of  the  Amoeba  becomes  free  from  the  sub- 
stratum. Now  as  the  Amoeba  passes  forward  the  particle  is  carried  to  the  upper 
surface,  as  shown  at  6.  (Thence  it  continues  forward  and  again  passes  beneath 
the  Amoeba,  etc.)  The  broken  lines  show  that  part  of  the  surface  of  the  Amoeba 
which  is  at  rest. 


THE   MOVEMENTS   AND   REACTIONS    OF   AMCEBA.  I4I 

(Fig.  38,  anterior  end) .     Further,  such  particles,  after  making  one  or 
two  revolutions,  usually  become  detached  and  drop  off. 

It  is  thus  clear  that  Amoeba  verrucosa  and  its  relatives  have  what 
may  be  called  a  rolling  motion ;  a  given  spot  on  the  outer  pellicula 
passes  forward  on  the  upper  surface,  downward  at  the  anterior  end, 
remains  quiet  on  the  lower  surface,  passes  upward  at  the  posterior 
end,  and  again  forward.  Its  movement  may  be  compared  directly  with 
the  movement  of  a  given  point  on  the  circumference  of  a  wheel  that  is 
rolling  forward.  A  diagram  of  the  movement  of  a  particle  on  the 
surface  as  it  would  appear  in  a  side  view  is  given  in  Fig.  40. 

Certain  details  of  the  movements  are  interesting,  and  may  best  be 
brought  out  by  description  of  specific  observations.  In  one  case  two 
small  particles  had  become  attached,  a  short  distance  apart,  to  the  surface 
of  a  specimen  of  Amoeba  sfhceronucleolus.  They  were  at  first  side  by 
side  and  a  little  to  the  right  of  the  middle  line,  one  somewhat  farther 
to  the  right  than  the  other  (Fig.  41).  They  moved  forward  in  parallel 
courses,  and  reached  the  anterior  edge  at  the 
same  time,  passing  over  the  edge  and  to  the 
under  surface.  It  now  required  two  and  one- 
half  minutes  for  the  Amoeba  to  pass  over  J) 
them,  during  which  time  they  remained  nearly 
or  quite  at  rest.  They  then  moved  upward 
to  the  upper  surface  and  forward  again.  The 
one  nearer  the  middle  line  moved  a  little 
faster  than  the  other,  reaching  the  anterior  edge  in  two  and  three- 
quarter  minutes,  while  the  lateral  one  required  three  minutes.  Both 
emerged  at  the  posterior  end  again  at  the  same  time,  the  central 
one  having  remained  quiet  three  and  one-fourth  minutes,  while  the 
lateral  one  had  been  three  minutes  at  rest.  The  next  forward  course 
required,  respectively,  but  one  and  one-half  and  two  minutes,  the  central 
particle  movmg  the  more  rapidly.  The  two  particles  were  no  longer 
side  by  side,  the  central  one  being  now  a  little  in  advance.  The  latter 
spent  after  the  next  turn  two  and  one-half  minutes  on  the  under  surface, 
while  the  lateral  particle  spent  but  two  minutes,  so  that  they  came  up 
from  the  posterior  end  again  at  the  same  time. 

The  two  particles  started  forward  again  and  had  reached  the  middle 
of  the  upper  surface  when  the  Amoeba  ceased  its  forward  movement, 
loosened  its  anterior  end  from  the  bottom,  and  became  attached  by  its 
posterior  end.     After  five  minutes  it  began  to  move  again,  but  now  in 


♦Fig.  41. — Paths  of  two  particles  attached  to  the  outer  surface  of  Amoeba 
sphcsr 01111  cleolus  as  described  in  the  text.  That  portion  of  the  paths  which  is  on 
the  lower  surface  is  represented  by  broken  lines.  (No  attempt  is  made  to  rep- 
resent the  forward  movement  of  the  Amoeba  in  this  figure.) 


142  THE   BEHAVIOR    OF   LOWER    ORGANISMS. 

the  opposite  direction,  so  that  the  former  posterior  end  became  anterior. 
At  the  same  time  the  two  particles  reversed  their  former  motion  and 
began  to  travel  back  in  the  direction  from  which  they  had  come — that 
is,  toward  the  new  anterior  end.  They  were  observed  to  make  several 
complete  turns  about  the  Amoeba  while  moving  in  this  new  direction. 
I  will  not,  however,  add  further  details,  as  those  above  recounted  are 
sufficient  to  give  a  conception  of  the  main  features  of  the  movement. 

Thus  two  definite  points  on  the  surface  of  an  Amoeba  may  retain 
nearly  the  same  relation  to  one  another  for  five  or  six  complete  revolu- 
tions, though  their  distance  apart  and  their  relative  position  may  vary 
a  little.  The  reversal  of  the  direction  of  rotation  when  the  direction  of 
locomotion  is  reversed,  described  in  the  above  case,  I  have  seen  many 
times. 

The  direction  of  the  movement  of  particles  on  the  outer  surface  is 
the  same  as  that  of  the  underlying  particles  of  endosarc.  The  rate  is 
also  about  the  same  as  for  the  endosarc,  though  often,  or  perhaps 
usually,  the  outer  particles  move  a  little  more  slowly  than  those  in  the 
endosarc. 

It  is  not  merely  a  thin  outer  layer  that  has  the  rolling  movement. 
This  is  demonstrated  by  the  movements  of  bodies  that  are  partly 
embedded  in  the  substance  of  the  Amoeba.  For  example,  a  large 
Euglena  cyst  had  become  attached  to  the  hinder  end  of  an  Amoeba 
sphceronucleolus.  The  cyst  was  carried  upward  and  forward  on  the 
upper  surface,  and  at  the  same  time  it  began  to  sink  into  the  protoplasm, 
so  that  when  it  had  reached  the  anterior  edge  it  was  partially  embedded. 
It  was  then  rolled  under,  remained  at  rest  on  the  under  surface  in  the 
usual  way,  and  came  up  at  the  posterior  end.  It  was  now  deeply  sunk 
in  the  protoplasm,  yet  it  moved  forward  in  the  usual  way.  By  the 
time  it  had  reached  the  anterior  edge  again  it  no  longer  protruded 
above  the  surface  at  all.  After  turning  the  anterior  edge  again  it  sank 
completely  into  the  body,  still  surrounded  by  a  la3'er  of  ectosarc,  so 
that  it  passed  to  the  interior  of  the  AmcEba  as  a  food  body.  I  have 
repeatedly  seen  bodies  which  were  thus  carried  forward  on  the  upper 
surface  gradually  taken  in  as  food.  They  always  continue  the  forward 
movement  even  when  completely  embedded  in  the  ectosarc.  It  is  thus 
evident  that  the  whole  thickness  of  the  ectosarc  partakes  of  the  forward 
movement.  The  forward  stream  in  ectosarc  and  endosarc  are  one  and 
continuous. 

The  relation  of  the  movements  of  the  outer  layer  to  the  lines  and 
wrinkles  seen  on  the  upper  surface  of  Amoeba  verrucosa  and  its  rela- 
tives is  of  interest.  There  are  usually  two  sets  of  these  wrinkles,  one 
set  diverging  from  the  posterior  end  toward  the  direction  in  which  the 
animal  is  moving,  the  other  set  forming  a  number  of  curved  lines 


THE    MOVEMENTS    AND    REACTIONS    OF   AMOEBA.  I43 

parallel  to  the  advancing  edge  (Fig.  38).  These  wrinkles  and  the 
areas  which  they  enclose  do  not  change  markedly  as  the  Amoeba 
advances,  so  that  the  outer  surface  of  the  body  seems  to  be  quite  at 
rest.  It  is  this  fact,  I  believe,  that  has  prevented  the  true  nature  of 
the  movement  in  these  species  from  being  recognized  before.  Thus 
Penard  (1902,  p.  118),  after  a  thorough  study,  accurate  so  far  as  it 
goes,  of  the  movements  of  Amoeba  verrucosa^  notes  that  many  facts 
point  to  the  existence  of  a  permanent  contractile  outer  layer,  but  holds 
that  the  permanence  of  certain  lines  and  patterns  on  the  upper  surface 
in  a  moving  Amoeba  is  crucial  against  the  idea  of  a  rolling  movement 
such  as  I  have  shown  above  to  actually  occur.  In  reality  these 
wrinkles  are  not  static  structures,  but  dynamic,  /.  ^.,  the  substance  of 
which  they  are  formed  is  in  continual  motion ;  they  are  like  the  per- 
manent ripples  on  the  surface  of  a  stream  where  the  latter  crosses  an 
obstruction.  The  wrinkles  indicate  the  direction  of  movement  of  the 
substance,  the  longitudinal  wrinkles  being  parallel  to  the  lines  of  motion, 
the  others  transverse  to  them.  A  particle  on  the  upper  surface  may 
move  parallel  with  the  longitudinal  wrinkles,  at  a  constant  distance 
from  them,  or  it  may  move  directly  along  one  of  these  wrinkles,  for 
the  whole  length  of  the  latter.  On  coming  to  one  of  the  transverse 
wrinkles  the  particle  moves  over  it  with  a  sort  of  jerk,  as  if  it  had 
passed  over  a  ridge  or  step,  as  indeed  it  has.  Thus  the  lines  and  the 
areas  enclosed  by  them  remain  constant,  while  the  substance  of  which 
they  are  composed  moves  onward. 

When  the  Amoeba  changes  in  a  marked  degree  its  direction  of 
movement,  so  as  to  follow,  for  example,  a  course  at  right  angles  to  the 
previous  one,  the  wrinkles  on  the  surface  usually  slowly  disappear,  then 
after  the  movement  has  become  well  established  in  the  new  direction, 
new  wrinkles  appear  in  correspondence  with  the  movement. 

When  such  a  change  of  course  occurs,  any  particles  on  the  upper 
surface,  which  were  moving  toward  the  anterior  edge,  change  their 
course  in  correspondence  with  the  new  direction  of  progression.  Fig. 
42  represents  a  case  of  this  kind,  where  an  Amoeba  verrucosa  bore  on 
its  upper  surface  a  minute  particle  of  debris  {a)  and  a  spherical  cyst  of 
Euglena  {b).  Both  moved  forward  over  the  stretch  x-y  (Fig.  42,  A), 
Now  a  little  methyl  green  (m)  was  allowed  to  diffuse  against  the  left 
side  of  the  Amoeba.  The  animal  changed  its  course,  moving  to  the 
right  At  the  same  time  the  two  objects  a  and  b  changed  their  direction 
of  movement,  traversing  the  stretch  ^-^r  (Fig.  42,  B)  until  they  reached 
the  new  anterior  edge  of  the  Amoeba,  and  were  carried  underneath. 

The  free-moving  (upper)  surface  and  the  resting  (lower)  one  in 
contact  with  the  substratum  may  exchange  roles  at  any  time  when 
the  contact  with  the  substratum  is  changed.    Thus,  a  specimen  was 


144 


THE    BEHAVIOR   OF    LOWER    ORGANISMS. 


creeping  on  the  slide  and  bearing  on  its  upper  surface  a  small  granule, 
which  was  moving  forward  in  the  usual  way.  The  Amoeba  stopped 
and  raised  its  anterior  edge,  which  came  in  contact  with  the  cover 
glass ;  it  then  loosened  itself  entirely  from  the  slide,  while  its  upper 
surface  became  attached  to  the  cover.  It  now  began  to  move  forward 
on  the  cover  glass.  The  granule  on  the  upper  surface  now  remained 
quiet,  until  it  was  reached  by  the  posterior  end,  when 'it  passed  down- 
ward to  the  lower  free  surface,  there  moving  forward  in  the  usual  way. 
Upper  and  lower  surfaces  had  completely  exchanged  roles.  In  a  sim- 
ilar way  I  have  seen  the  thin  lateral  edge  of  a  specimen  become  the 
middle  of  the  upper  moving  surface. 

Objects  of  the  most  varied  sort  cling  to  the  surface  of  Amoeba  verru- 
cosa and  its  relatives.  I  have  seen  the  following  attached  to  the  surface 
and  showing  the  typical  movements :  Particles  and  masses  of  soot, 
granules  of  India  ink,  motionless  bacteria,  diatom  shells,  dead  flagel- 
lates, masses  of  debris, 
cysts  of  Euglena,  a  small 
Amoeba  proteus  (the  lat- 
ter was  inclosed  after  it 
had  passed  to  the  under 
surface).  Usually  only 
one  or  two  small  objects 
are  seen  attached  to  any 
given  specimen,  but  to 
this  extent  the  phenomenon  is  very  common,  so  that  it  seems  rather 
surprising  that  the  movements  of  such  particles  should  not  have  been 
described  before. 

A  number  of  other  points  must  be  set  forth  before  we  can  form  a 
clear  conception  of  the  movements  of  these  Amoebae.  The  species 
under  consideration  are  much  flattened  and  have  usually  an  oval  form 
as  they  move  forward,  the  anterior-posterior  axis  being  the  longer, 
while  the  posterior  end  is  the  more  pointed  (Fig.  38).  Not  the  whole 
lower  surface  is  in  contact  with  the  substratum,  but  only  a  band  at  the 
anterior  and  lateral  margins.     In  an  Amoeba  that  was  creeping  on  the 


Fig.  42.* 


*  Fig.  42. — Movement  of  bodies  attached  to  the  surface  in  Amoeba  verrucosa, 
when  the  direction  of  locomotion  is  changed,  a,  P^  small  granule  ;  b,  a  Euglena 
cyst.  In  A  the  Amoeba  is  progressing  to  the  right,  as  shown  bj  the  large  arrow ; 
the  two  bodies  attached  to  the  surface  moved  in  the  same  direction,  traversing 
the  stretch  x-y,  as  shown  bj  the  small  arrows.  At  this  point  a  solution  of 
methyl  green  (;«)  was  allowed  to  diffuse  against  the  surface ;  the  Amoeba  there- 
upon changed  its  course,  as  indicated  by  the  large  arrow  of  ^.  At  the  same 
time  the  bodies  a  and  b  changed  their  course,  traversing  the  stretch  y-z.  The 
stretch  x-y-z  in  B  shows  thus  the  path  of  the  attached  bodies  before  and  after 
the  reaction. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I45 

lower  surface  of  the  cover  glass  I  was  able  to  define  with  some  accuracy 
the  parts  that  were  attached  and  those  that  were  not.  A  small  flagel- 
late was  moving  briskly  about  between  the  Amoeba  and  the  cover  glass, 
but  its  excursions  were  limited  by  a  visible  line  running  parallel  with 
the  anterior  edge  of  the  Amoeba  and  extending  at  the  sides  back  to 
about  one-third  the  animal's  length  from  the  rear  (Fig.  43,  a-a-a). 
The  zone  between  this  and  the  margin  was  pressed  close  to  the  glass, 
and  was  evidently  attached  to  it  The  more  pointed  posterior  end  was 
held  quite  away  from  the  glass,  leaving  a  broad  passageway  through 
which  the  flagellate  finally  escaped. 

The  results  of  this  observation  were  confirmed  by  another.  An 
Amoeba  verrucosa  in  full  career  was  suddenly  turned  on  one  lateral 
edge  by  a  strong  current  from  a  rotifer,  and  its  upper  edge  coming  in 
contact  with  the  cover,  glass,  it  remained  in  that  position  sometime 
without  change  of  form.  It  could  be  seen  that  the  under  surface  was 
concave,  the  edges  very  thin  and  flat,  while  the 
posterior  portion  was  thick  and  arched  (Fig.  44). 

It  is  clearly  at  the  advancing  edge  of  the  ani- 
mal that  the  most  active  movements  are  taking 
place.  Here  the  hyaloplasm  may  be  seen  to 
push  forward  in  a  series  of  short  waves,  the 
anterior  edge  of  each  becoming  attached  to  the 
substratum.  At  the  same  time,  of  course,  an 
equivalent  amount  of  protoplasm  becomes  de- 
tached from  the  substratum  along  the  line  a-a-a^ 
Fig.  43,  though  this  does  not  take  place  in 
waves,  so  far  as  observable.  The  anterior  wave  must  in  some  way 
pull  upon  the  upper  surface  of  the  Amoeba,  bringing  it  forward,  and 
dragging  with  it  the  elevated  sac-like  posterior  end.  A  certain  feature 
of  the  advance  of  the  anterior  edge  seems  of  much  significance.  Each 
wave  seems  to  arise  just  behind  the  previous  anterior  boundary  line 
and  overlaps  it,  leaving  it  buried.  This  line  often  remains  visible  for 
a  short  time  after  the  new  wave  has  been  formed.  The  new  wave 
rolls  over  the  preceding  one  in  such  a  way  that  its  original  upper 
surface  becomes  applied  to  the  substratum.  This  is  demonstrated  by 
the  rolling  under  of  small  objects  on  the  upper  surface  of  the  advanc- 
ing wave.  A  diagram  of  the  movement  at  the  anterior  edge  is  given 
in  Fig.  45.  The  movement  can  be  imitated  roughly  by  making  a 
cylinder  of  cloth,  laying  it  flat  on  a  plane  surface,  and  pulling  forward 

*  Fig.  43. — Attached  surface  oiAmceba  verrucosa,  creeping  on  the  lower  surface 
of  the  cover  glass.  The  unshaded  portion  in  front  of  the  line  a-a-a  is  attached 
to  the  substratum,  while  the  shaded  portion  is  free  and  raised  slightly  above 
the  substratum. 


146  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  anterior  edge  in  a  series  of  waves.     The  entire  cylinder  then  rolls 
forward  just  as  the  Amoeba  does. 

The  essential  features  of  the  movement  seem  to  be  (i)  the  advance  of 
the  wave  from  the  upper  surface  at  the  anterior  edge  ;  (2)  the  pull  exer- 
cised by  this  wave  on  the  remainder  of  the  upper  surface  of  the  body, 
bringing  it  forward.  Most  of  the  other  phenomena  follow  as  conse- 
quences of  these  two.  The  flowing  forward  of  the  granules  of  the 
endosarc  seems  to  demand  no  special  explanation,  since  a  fluid  con- 
taining granules  within  a  rolling  sac  must  necessarily  flow  forward  as 
the  sac  rolls.  By  the  movement  forward  of  the  anterior  end  a  space  is 
left  free  ;  by  the  rolling  forward  of  the  posterior  end  the  fluid  is  piled 
up  and  pressed  upon,  and  must  flow  forward  into  the  empty  space  in 
front.  Possibly  there  may  be  other  causes  at  work  in  producing  the 
endosarcal  currents,  but  such  currents  would  be  produced  without 
other  cause  in  a  sac  moving  as  Amoeba  does. 


^ 

\ 

a 

h 

Fig.  44.*  Fig.  45.! 

other  species  of  amoeba. 

Thus  far  we  have  dealt  only  with  Amoebae  of  rather  constant  form, 
which  do  not  produce  pseudopodia,  or  only  rarely  do  so.  We  must  now 
take  up  species  in  which  the  form  is  changeable  and  the  movements 
varied.  Of  such  species  I  have  studied  chiefly  Amoeba  limax^  A. 
proteus^  and  a  smaller  Amoeba,  which  I  take  to  be  Amoeba  angulata 
Meresch.  In  these  species  the  outer  surface  is  not  viscid,  except  at  the 
posterior  end,  so  that  small  objects  rarely  cling  to  it.  It  is,  therefore, 
much  more  difficult  to  determine  the  direction  of  movement  of  the 
upper  surface  than  in  Amoeba  verrucosa  and  its  relatives.  Yet,  by 
mixing  soot  with  the  water,  and  devoting  a  sufficient  amount  of  time 
and  patience  to  the  work,  one  can  obtain  as  many  observations  as  he 
desires.     The  soot  settles  upon  the  upper  surface  in  particles  or  masses 


♦Fig.  44. — Side  view  (partly  an  optical  section)  of  a  creeping  Amosba  verru- 
cosa^ showing  the  thin  anterior  edge  (/I)  attached  to  the  substratum,  and  the 
high  posterior  portion  (/*)  with  a  cavity  beneath  it. 

t  Fig.  45. — Diagram  of  the  movement  at  the  anterior  edge  of  Amoeba  verrucosa. 
The  region  h-c  pushes  out,  taking  up  the  position  b'-c\  and  pulling  forward  the 
region  c-</,  so  that  it  comes  to  occupy  the  position  c'-d' .  The  point  a  remains 
in  its  place. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMOEBA.  I47 

and  its  movements  can  be  followed  ;  at  times,  also,  objects  actually 
cling  to  the  surface,  as  in  the  other  species. 

The  results  are  essentially  the  same  as  in  the  species  already  described  ; 
foreign  particles  resting  upon  or  clinging  to  the  upper  surface  are  car- 
ried forward  to  the  anterior  edge.  Here  they  roll  over  the  edge,  passing 
beneath  the  Amoeba,  which  now  moves  across  them.  As  a  rule  in 
these  species  particles  do  not  cling  to  the  surface  after  passing  to  the 
lower  side,  so  that  they  are  left  behind  when  the  posterior  end  passes 
over  them.  Sometimes  they  do  thus  cling,  however,  and  in  such  cases 
I  have  seen  them  pass  upward  at  the  posterior  end  and  again  forward, 
exactly  as  in  A.  verrucosa  and  its  relatives.  In  order  that  my  state- 
ments may  not  remain  abstract  and  general,  I  copy  a  few  observations 
from  my  notebook,  all  relating  to  Amoeba  proteus. 

1.  A  large  particle  of  debris  with  bits  of  soot  attached  to  it  was  seen 
lying  on  the  upper  surface  just  behind  the  middle.  It  was  carried 
forward  to  the  anterior  end  and  over  the  edge.  Then  it  came  to  rest 
on  the  bottom,  and  the  Amoeba  crept  over  it  till  it  was  passed  by  the 
posterior  end  and  left  behind. 

2.  A  number  of  soot  particles  on  the  upper  surface  just  in  front  of 
the  middle  were  carried  forward,  changing  their  direction  as  the  proto- 
plasmic currents  beneath  them  changed  direction.  They  were  finally 
carried  over  the  anterior  edge. 

3.  A  small  mass  of  soot  was  lying  on  the  middle  of  the  upper  surface. 
It  moved  forward  in  the  same  way  as  the  endosarcal  granules  under- 
neath. The  latter  changed  their  direction  of  movement  several  times  ; 
the  soot  mass  changed  correspondingly  at  the  same  time.  It  was 
finally  carried  over  the  anterior  edge,  where  it  could  be  seen  clearly 
separate  from  the  Amoeba. 

4.  A  large  mass  of  soot  one-quarter  the  size  of  the  Amoeba  was 
carried  forward  on  the  upper  surface  for  a  distance,  but  fell  off'  at  the 
side  before  reaching  the  anterior  end. 

5.  Two  small  masses  of  soot  lying  on  the  upper  surface  of  the 
posterior  end  were  carried  forward  over  the  anterior  edge. 

6.  Several  small  particles  were  clinging  to  the  lower  surface  of  the 
posterior  end.  They  passed  upward,  one  of  them  around  the  very 
middle  of  the  posterior  end,  to  the  upper  surface ;  here  they  were 
carried  forward  and  over  the  anterior  edge. 

I  could  add  a  large  number  of  such  observations. 

On  the  under  surface  the  particles  are  quiet,  as  I  have  shown  before 
(p.  136).  At  the  lateral  margins  the  edges  of  this  quiet  lower  surface 
are  seen,  so  that  particles  situated  here  are  usually  likewise  quiet,  until 
they  have  reached  the  posterior  part  of  the  Amoeba  (see  p.  135). 

As  to  the  details  of  the  movement  of  the  upper  surface,  the  following 


I4S  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

are  important.  Particles  situated  on  the  upper  surface  move  usually 
at  the  same,  or  nearly  the  same,  rate  as  the  granules  beneath  them,  in 
the  endosarc.  The  movement  of  the  surface  particles  follows  exactly 
that  of  the  endosarc  beneath  them,  changing  in  direction  when  the  latter 
changes.  Two  particles  close  together  on  the  upper  surface  may  thus 
diverge  or  even  flow  in  opposite  directions,  carried  by  two  different 
currents  which  are  visible  in  the  endosarc.  Any  portion  of  the  ecto- 
sarc,  like  any  portion  of  the  interior,  may  stop  at  any  time,  while  other 
parts  flow  onward.  One  may  thus  see  at  times  a  particle  at  rest  on  the 
upper  surface  of  a  moving  Amoeba.  Isolated  observations  of  this  kind 
might  lead  one  to  suppose  that  the  upper  surface,  like  the  lower,  remains 
at  rest  while  the  endosarc  passes  forward.  But  when  a  particle  on  the 
surface  is  at  rest,  one  will  usually  find,  by  a  proper  change  of  focus, 
that  the  endosarc  beneath  it  is  likewise  at  rest.  It  is,  of  course,  well 
known  that  certain  portions  of  the  endosarc  may  be  at  rest  while  the 
remainder  is  in  movement  (see  Rhumbler,  1898,  p.  122).  In  the  same 
way  a  portion  of  the  outer  layer  may  sometimes  be  at  rest  while  the 
adjacent  endosarc  is  in  motion  ;  this,  however,  is  rather  unusual. 

We  may  sum  up  our  results  thus  far  in  the  following  statements : 
In  an  advancing  Amoeba  substance  Jloivs  forward  on  the  upper  sur- 
face^ rolls  over  at  the  anterior  edge^  coming  in  contact  with  the 
substratum^  then  remains  quiet  until  the  body  of  the  Amoeba  has 
passed  over  it.  It  then  moves  upward  at  the  posterior  end.,  and 
forward  again  on  the  upper  surface.,  continuing  in  rotation  as  long 
as  the  Amoeba  continues  to  progress.  The  motion  of  the  upper 
surface  is  congruent  with  that  of  the  endosarc,  the  two  forming  a 
single  stream. 

HISTORICAL,    ON    ROLLING    MOVEMENTS    IN    AMOEBA. 

The  possibility  that  Amoeba  progresses  by  a  rolling  movement  was 
discussed  by  Claparede  &  Lachmann  (1858).  In  Amoeba  Umax  and 
Amoeba  quadrilineata  (==  A.  verrucosa) .,  according  to  these  authors, 
the  general  appearance  of  locomotion  is  in  many  respects  in  favor  of 
this  view  :  "  On  croit  positivement  voir  Tanimal  rouler  sur  lui-meme  " 
(p.  435).  But  this  correct  view  is  rejected  (in  the  text)  because  of  the 
(supposed)  permanence  in  the  position  of  the  contractile  vacuole. 
Claparede  &  Lachmann  insist  that  the  contractile  vacuole  is  situated 
in  the  ectosarc  ;  hence,  they  argue,  if  there  were  a  rolling  movement 
of  the  ectosarc,  the  vacuole  would  necessarily  partake  of  the  movement ! 
In  a  note  on  p.  437  it  is  stated,  however,  that  Lachmann  personally 
believed  the  motion  to  be  of  this  rolling  character.  "  II  croit  s'etre 
assur^  que  V A.  quadrilineata  roule  sur  elle-meme."  According  to 
Claparede  &  Lachmann,  Perty  held  this  view  also. 


THE    MOVEMENTS    AND    REACTIONS    Oi^    AMCEBA.  t^g 

Dr.  Wallich  shared  the  correct  opinion  of  Lachmann  and  Party. 
This  excellent  observer  unfortunately  often  gave  his  results  in  the  form 
of  mere  brief  general  statements,  so  that  one  cannot  judge  how^  much 
evidence  he  had  for  them,  and  little  attention  has,  therefore,  been  paid 
them.  But  it  is  singular  how  many  of  these  statements  show  them- 
selves to  be  correct,  even  in  opposition  to  later  work.  Concerning 
the  matter  in  question,  Wallich  has  the  following: 

In  short  the  effect  is  similar  to  that  which  would  be  produced  were  an  empty 
and  transparent  bladder  or  caoutchouc  sac,  containing  granular  bodies  of  greater 
specific  gravity  than  the  viscid  fluid  within  which  they  were  sustained,  to  be 
rolled  along  a  plain  surface.     (Wallich,  1863,  b,  p.  331.) 

He  makes  no  attempt  to'  demonstrate  the  truth  of  this  correct  com- 
parison, and  does  not  develop  the  matter  beyond  the  mere  statement 
given  above. 

Schulze  (1S75),  Berthold  (1886),  and  Biitschli  (1892),  as  we  have 
seen,  agree  in  stating  that  the  currents  on  the  upper  surface  at  the 
anterior  end  in  Pelomyxa  are  backward.  In  view  of  the  great  authority 
of  these  writers  we  should  be  compelled  to  suppose  that  the  movement 
in  this  animal  is  of  an  entirely  different  character  from  that  found  in 
the  various  species  of  Amoeba,  but  for  a  most  fortunate  circumstance. 
The  only  previous  demonstrated  observation  of  the  forward  movement 
of  the  upper  surface  in  the  Rhizopoda  relates  precisely  to  Pelomyxa, 
and  was  made  by  an  investigator  closely  associated  with  Biitschli. 
It  was  not  until  my  work  was  finished  and  the  present  paper  written 
that  I  came  across  the  note  of  Blochmann  (1S94)  on  the  movements  of 
Pelomyxa.  Blochmann  shows  that  the  movement  of  substance  on  the 
upper  surface  of  Pelomyxa  is  forward,  just  as  we  have  found  it  to  be 
in  Amoeba.  The  outer  surface  of  Pelomyxa  is  covered  with  fine  cilia- 
like  projections.  By  observing  these  projections  Blochmann  had  no 
difficulty  in  seeing  that  they  move  forward  on  the  upper  surface.  The 
rate  of  movement  was  the  same  as  that  of  the  internal  forward  current. 
Biitschli  (1893,  Appendix,  p.  220)  had  already  observed,  greatly  to  his 
surprise,  that  there  is  a  forward  current  in  the  water  next  to  the  sur- 
face of  an  advancing  Pelomyxa,  this  current  being  exactly  the  reverse 
of  that  called  for  by  the  theory  that  the  motion  is  due  to  a  lowering  of 
the  surface  tension  at  the  anterior  end. 

Biitschli  (/.  c.)  attempted  to  save  the  surface  tension  theory  by  sug- 
gesting that  it  was  only  a  thin  outer  layer  that  moves  forward.  The 
currents  in  the  moving  animal  would  then  be  as  follows :  A  forward 
current  within,  a  backward  current  just  beneath  the  surface,  a  forward 
current  in  a  thin  layer  on  the  surface.  It  is  possible  that  this  compli- 
cated arrangement  of  currents  might  be  brought  into  harmony  in  some 
way  with  the  surface-tension  theory  of  the  movement,  though  it  is 


150  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

rather  difficult  to  see  how  the  forward  movement  of  the  outer  layer 
would  be  produced.  As  we  have  seen,  Blochmann  found  that  the 
internal  and  external  forward  currents  move  at  the  same  rate  and  in 
the  same  direction.  It  is  difficult  to  explain  how  this  should  occur  if 
the  two  are  separated  by  a  layer  moving  in  the  opposite  direction. 
But  Blochmann  accepted  Biitschli's  suggestion,  and  attempted  to  give 
some  evidence  in  its  favor.  He  says  that  one  sees  the  outer  current, 
with  the  movement  of  the  projections,  in  places  where  the  marginal 
current  has  come  to  rest,  and  that  the  outer  and  internal  currents  then 
move  at  the  same  rate,  separated  by  the  resting  marginal  layer.  Now 
one  can  receive  exactly  this  impression  in  Amoeba  in  the  following 
manner :  The  margins  where  they  are  pressed  against  the  substratum 
are  at  rest.  Just  above  this  region,  and  often  visible  in  the  same  focus, 
there  is  the  forward  current,  which  is  visible  on  the  one  hand  on  the 
surface  (through  the  movements  of  the  projections) ;  on  the  other  hand, 
in  the  interior  (through  the  movements  of  the  granules  of  the  endosarc). 
Unless  one  is  on  his  guard  as  to  the  slight  difference  in  level,  one  might 
seem  to  see  two  currents  separated  by  a  resting  layer,  particularly  if 
the  probability  that  this  were  true  had  been  suggested  beforehand.  It 
is  notable  that  Blochmann  describes  nowhere  outer  and  inner  forward 
currents,  separated  by  a  marginal  backward  current,  as  would  be 
required  by  the  modified  surface-tension  theory. 

We  have  demonstrated  above,  for  Amoeba  at  least,  that  the  forward 
movement  is  not  confined  to  a  thin  outer  layer,  but  extends  from  the 
outer  surface  to  the  endosarc  (p.  142) ;  in  other  words,  that  the  outer 
surface  moves  in  continuity  with  the  internal  substance. 

Rhumbler  (1898,  pp.  126-130)  discussed  at  length  the  possibility  of 
explaining  the  movement  of  Amoeba  by  means  of  a  rolling  sac  of 
ectoplasm,  only  to  come  to  the  conclusion  that  it  was  impossible. 
Rhumbler's  discussion  of  this  matter  is  an  excellent  example  of  the 
fact  that  acumen  and  excellent  reasoning  may  lead  one  astray  in  scien- 
tific matters  when  the  observational  basis  for  the  reasoning  is  not 
secure.  What  chiefly  misled  him  was  an  incorrect  idea  as  to  the 
direction  of  the  currents  in  the  substance  of  Amoeba,  particularly  his 
assumption  that  there  is  a  backward  current  on  the  upper  surface. 
The  diagram  which  he  gives  of  the  currents  as  they  must  occur  in  an 
Amoeba  moving  in  a  rolling  manner  (Fig.  33,  A,  p.  133)  is,  therefore, 
much  more  nearly  correct  than  that  in  which  he  shows  what  he  con- 
siders the  really  existing  currents  (Fig.  33,  jS), 

Rhumbler's  conception  as  to  the  necessary  movements  in  the  sub- 
stance of  an  Amoeba  progressing  by  rotation  is,  however,  incorrect  in 
one  particular,  so  that  his  diagram  (Fig.  33,  A)  does  not  correspond 
to  the  facts  in  this  point.     He  assumes  that  there  must  be  a  backward 


THE    MOVEMENTS   AND    REACTIONS    OF   AMCEBA.  15I 

current  on  the  lower  surface,  as  indicated  by  the  lower  (heavier)  arrows 
in  his  diagram  (Fig.  33,  A).  This  backward  current  does  not  exist, 
and  is  theoretically  unnecessary,  as  may  be  seen  by  making  a  cylinder 
of  cloth  and  moving  it  in  the  manner  described  above  (p.  145).  The 
under  surface  remains  at  rest  until  it  passes  upward  at  the  posterior 
end  {cf.  Fig.  40) .  Rhumbler  held  that  this  backward  current  below, 
with  the  forward  current  above  (Fig.  33,  A),  must  set  the  endosarc 
in  rotation  ;  "  the  endoplasma  granules  would  themselves  necessarily 
all  move,  like  the  particles  of  the  ectosarc,  in  circular  or  elliptical 
courses"  (p.  128).  The  absence  of  such  circular  or  elliptical  paths  for 
the  granules  of  the  endosarc  would  then  speak  against  the  method  of 
movement  by  rotation  of  the  ectoplasm.  But  since  there  is  no  such 
backward  current  as  Rhumbler  assumes,  and  not  even  the  particles  of 
the  ectosarc  move  in  circular  or  elliptical  courses,  this  objection  falls 
to  the  ground. 

Further,  Rhumbler  seems  to  assume  that  for  locomotion  by  a  rotary 
movement  of  the  ectosarc,  the  latter  must  necessarily  be  a  "sharply 
defined  persistent  organ,"  and  that  its  contractions  could  only  be  due 
to  preformed,  permanent  fibers,  in  a  definite  arrangement.  Rhumbler 
is  able  to  show  of  course  that  these  two  assumptions  are  probably  incor- 
rect, and  considers  that  this  weighs  against  the  possibility  of  movement 
in  the  manner  characterized.  But  both  these  assumptions  are  unneces- 
sary. The  rotation  demonstrably  does  occur,  yet  the  permanent,  sharply 
defined  ectosarc  with  definitely  arranged  persistent  fibers  does  not  exist, 
as  Rhumbler  has  set  forth,  and  as  must  be  evident  to  anyone  who 
studies  for  a  long  time  the  changes  of  form  and  movement  in  Amoeba. 
As  we  shall  see  later,  a  simple  drop  of  fluid,  with  no  differentiated  outer 
layer,  may  move  in  the  same  manner. 

Penard  (1902)  also  discusses  the  possibility  of  movement  by  rotation 
of  the  ectosarc  in  Amceda  verrucosa  (==  A.  terricold) .  His  study  of 
the  movements  is  excellent  and  he  gives  as  a  possibility  on  p.  115  what 
is  really  in  its  main  features  a  nearly  accurate  statement  of  the  method 
in  which  locomotion  actually  occurs,  only  to  reject  this  possibility  later. 
The  ground  for  this  rejection  is  as  follows :  The  posterior  end  of  the 
Amoeba  often  bears  an  irregular  saclike  projection  (what  Penard  calls 
the  "  houppe"  )  ;  this  may  be  much  wrinkled  or  covered  with  projec- 
tions. This  wrinkled  sac  retains  its  position  ;  in  Afnoeba  verrucosa  it 
is  covered,  like  the  rest  of  the  body,  with  a  resistant  cuticula,  which  can 
be  dissolved  only  with  great  difficulty  and  very  slowly. 

If  the  Amoeba  rolled  on  itself  in  progressing,  the  posterior  part  of  this  mem- 
brane would  necessarily  follow  the  movement  and  pass  little  by  little  forward, 
which  is  contrary  to  the  facts.  The  best  manner  of  assuring  one's  self  of  the 
immobility  of  the  pellicle  is  to  look  very  attentively  at  the  surface  of  the  con- 


152 


THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


tractile  vacuole;  there  one  sees  almost  always  very  fine  folds,  forming  angles 
and  varied  patterns;  these  angles  and  these  patterns  remain  for  a  long  time 
absolutely  the  same,  which  shows  that  nothing  has  changed  place.  (Penard, 
1902,  p.  118.) 

In  all  the  specimens  of  Amceda  verrucosa  and  A.  sphceronucleolus 
in  which  I  have  studied  the  matter,  the  posterior  part  of  the  outer  mem- 
brane does  follow  the  movement.  Particles  clins^ing  to  the  outer  surface 
of  the  hinder  part  of  the  ectosarc  pass  upward  over  the  wrinkled  sac- 
like posterior  end  and  forward  on  the  upper  surface.  In  so  doing  they 
pass  directly  across  the  wrinkles  on  the  body  sur- 
face, as  set  forth  on  p.  143.  Had  Penard  chanced  to 
^       -    ^  see  the  movements  of  a  particle  attached  to  the  outer 

surface  of  the  body  he  could  not  have  been  misled 
by  the  apparent  permanence  of  the  surface  wrinkles . 

FORMATION  AND  RETRACTION  OF  PSEUDOPODIA. 

Thus  far  the  phenomena  in  Afrioeba  froteus 
and  its  relatives  are  essentially  like  those  found 
in  Amceba  verrucosa.  At  times  Amoeba  proteus 
flows  forward  as  a  single  simple  mass  ;  then  its 
locomotion  may  be  compared  directly  in  its  chief 
features  to  that  of  Amoeba  verrucosa.  But  in 
Amoeba  proteus  and  its  relatives  the  movement 
is,  of  course,  usually  much  complicated  by  the  for- 
mation of  pseudopodia.  In  considering  the  way 
n  which  these  are  formed  we  must  deal  separately 
with  two  different  cases,  depending  on  whether  the 
pseudopodium  when  sent  out  is  or  is  not  in  contact 
with  the  substratum. 

SURFACE   CURRENTS    IN   THE    FORMATION   OF   PSEUDOPODIA 
IN   CONTACT   Vi^ITH   THE    SUBSTRATUM. 

Fig.  46.*  When  the  pseudopodium  is  sent  out  in  contact 

with  the  substratum,  the  phenomena  accompany- 
ing its  formation  are  essentially  the  same  as  those  which  take  place  at 
the  anterior  end  of  an  advancing  Amoeba ;  the  latter  may  indeed  be 
considered  as  merely  a  large  pseudopodium.     Even  when  the  pseudo- 


*  Fig.  46. — Movement  of  a  particle  attached  to  the  outer  surface  of  a  pseudo- 
podium that  is  extending  in  contact  with  the  substratum.  At  a  the  particle  is 
at  the  middle  of  the  upper  surface;  at  b  it  has  nearly  reached  the  tip.  When 
the  pseudopodium  has  reached  the  length  shown  at  c  the  particle  has  passed 
over  its  tip.  Here  it  remains,  so  that  at  d,  when  the  pseudopodium  has  become 
longer,  the  particle  is  still  at  the  same  level,  but  on  the  under  surface  of  the 
pseudopodium,  some  distance  behind  the  tip. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


'53 


podia  are  slender  and  pointed,  the  protoplasm  flows  forward  (toward 
the  point)  on  the  free  upper  surface  and  in  the  interior,  while  on  the 
side  which  is  in  contact  with  the  substratum  the  protoplasm  is  at  rest. 
I  have  often  seen  small  particles  which  had  been  brought  forward  on 
the  surface  of  the  Amoeba  carried  out  to  the  tip  of  a  pseudopodium  on 
its  upper  surface,  finally  rolling  over  the  point  and  becoming  covered 
by  the  advancing  protoplasm  (Fig.  46) . 

FORMATION    OF    FREE    PSEUDOPODIA. 

When  a  pseudopodium  is  sent  out  directly  into  the  water,  so  that  its 
surface  is  free  on  all  sides,  "it  is  much  more  difficult  to  determine  the 
nature  of  the  movement.  Particles  rarely  cling  to  the  surface  of  such 
a  pseudopodium,  and  without  this  aid  one  cannot  be  certain  what  the 
movement  of  the  outer  layer  is.  However,  by  devoting  several  entire 
days  under  most  favorable  conditions  to  the  determination  of  this  point, 
I  collected  a  number  of  observations  which  demonstrate  clearly  the 
nature  of  the  move- 
ment. The  point  \  a  ^  ^ 
of  special  interest 
is,  here  as  else- 
whe  re  ,  whether 
there  is  a  back- 
ward current  on 
the  surface  of  the 
advancing  pseudo- 
podium, as  repre- 
sented  in  the  dia- 


FiG.  47. 


gram  from  Rhumbler,  Fig.  31.  To  this  the  observations  give  a  negative 
answer.  Particles  clinging  to  the  surface  of  a  pseudopodium,  whether 
at  the  tip  or  at  the  base  or  at  any  intermediate  point,  are  uniformly 
carried  outward,  in  the  same  direction  as  the  tip.  Particles  situated  at 
a  certain  distance  from  the  tip  of  a  short  pseudopodium  maintain  the 
same  distance  as  a  rule  when  the  pseudopodium  is  lengthened,  though 
in  so  doing  they  are  carried  far  out  from  the  body.  Sometimes  the  tip 
moves  outward  a  little  faster  than  the  parts  behind  it,  the  pseudopodium 
thus  becoming  more  slender  as  it  extends,  but  all  parts  agree  in  being 
carried  outward.  A  number  of  examples  of  actual  observations  will 
make  this  point  clear. 

I.  Amoeba  angulata  :  When  first  observed  there  was  a  short  pseudo- 
podium in  front,  projecting  freely  into  the  water.  A  small  particle  was 
attached  to  the  surface  at  about  the  middle  of  its  length  (Fig.  47,  a), 

*  Fig.  47. — Successive  stages  in  the  formation  of  a  free  pseudopodium,  showing 
the  movement  of  a  particle  attached  to  its  surface.  The  particle  moves  outward, 
keeping  at  approximately  the  same  distance  from  the  tip. 


154  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  pseudopodium  lengthened,  carrying  the  particle  with  it,  the  latter 
maintaining  its  distance  from  the  tip  nearly  or  quite  constant,  but  being 
carried  far  from  the  body  (Fig.  47,  b).  The  pseudopodium  finally  became 
very  long  and  slender  (c),  the  particle  remaining  attached  near  the  tip. 

2.  Afiiceba  proteus :  A  particle  clinging  to  the  surface  of  one  side, 
near  the  anterior  end.  A  pseudopodium  was  formed  at  exactly  this 
point,  extending  freely  into  the  water,  so  that  the  particle  was  borne 
on  the  tip  of  the  pseudopodium.  It  maintained  this  position  while  the 
pseudopodium  was  extending,  and  was  still  found  at  the  tip  after  the 
pseudopodium  had  become  long  and  slender  (Fig.  48). 

The  third  example  which  I  give  is  one  of  much  interest,  because  it 
shows  the  movements  of  a  given  point  on  the  surface  in  both  the  retrac- 
tion and  extension  of  pseudopodia,  as  well  as  in  transference  from  the 
posterior  to  the  anterior  region  of  the  body. 

3.  A^nceba  proteus:   When  first  observed  the  animal  was  rather 

slender,  creeping  in  a  certain  direc- 
tion, and  with  two  long  pseudo- 
podia at  the  posterior  end,  extend- 
ing, one  on  each  side,  at  right 
angles  to  the  axis  of  progression 
(Fig.  49,  a).  The  left  pseudo- 
podium was  the  longer,  and  bore 
at  about  one-fourth  its  length  from 
its  base  a  small   particle   {x)   at- 

Pjq    .3  *  tached    to    its    surface   by  a  very 

short  stalk  in  such  a  way  that  it 
was  seen  in  profile  (Fig.  49,  a).  The  pseudopodium  was  not  in 
contact  with  the  bottom,  and  was  slowh^  retracting,  its  internal  con- 
tents flowing  into  the  body,  while  the  pseudopodium  itself  shortened. 
As  this  occurred  the  particle  approached  the  body  and  finally  passed 
on  to  its  surface  {b,  c)  while  the  pseudopodium  was  yet  of  considerable 
length.  It  was  evident  that  the  shortening  of  the  pseudopodium  took 
place  chiefly  at  its  base,  since  the  part  between  the  base  and  the  particle 
X  had  become  incorporated  with  the  body  when  the  portion  between  x 
and  the  tip  had  changed  only  a  little  in  length  {b,  c) .  This  distal 
portion  apparently  did  become  somewhat  shorter  at  the  same  time, 
while  its  surface  became  slightly  wrinkled.  By  the  time  the  tip  of  the 
pseudopodium  had  united  with  the  body  {d)  the  particle  x  had  moved 
a  considerable  distance  forward  on  the  latter.  The  posterior  portion 
of  the  body  was  here  thick,  and  the  particle  was  still  seen  in  profile, 
though  it  was  some  distance  above  the  substratum.     It  now  moved 


♦  Fig.  48. — Movement  of  a  particle  attached  to  surface  of  an  Amoeba  at  point 
where  a  free  pseudopodium  is  pushed  forth.     The  particle  remains  at  the  tip. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


155 


forward  very  slowly  (c,  d^  e)  till  at  f  it  passed  to  the  upper  surface. 
It  then  moved  rapidly  forward,  occupying  successively  the  positions 
indicated  by  the  line  of  circles  in  g:  (The  Amoeba  itself  was,  of  course, 
progressing  ;  no  attempt  is  made  in  the  diagram  to  represent  its  change 
of  position.)  Finally  the  particle  x  had  nearly  reached  the  anterior 
end,  when  the  latter  forked,  sending  two  pseudopodia  upward  and 
forward  into  the  water  (^,  h).  The  particle  x  was  at  first  at  the  base 
of  the  right  pseudopodium.  This  was  now  projected  forward  as  a  very 
long,  slender  pseudopodium  bearing  the  particle  x.  The  latter  was 
carried  steadily  out  from  the'  body,  maintaining  almost  exactly  its 
original  distance  from  the  tip  of  the  pseudopodium  {h^  i^j)-     It  is 


I 


Fig.  49* 

possible  that  as  the  tip  became  very  slender  its  distance  from  x  became 
slightly  greater  as  if,  by  a  circular  contraction  of  the  intervening  part, 
the  tip  were  forced  further  out ;  but  there  was  no  movement  backward 
of  :v;  on  the  contrary,  it  moved  steadily  forward,  its  distance  from  the 
base  of  the  pseudopodium  continually  increasing.  Unfortunately  at 
this  point  the  animal  passed  under  a  mass  of  debris,  so  that  I  was 
unable  to  trace  further  the  history  of  that  point  on  the  body  surface 
marked  by  the  particle  x. 

I  have,  altogether,  about  a  dozen  observations  showing  this  outward 
movement  of  particles  on  the  surface  of  free  pseudopodia.     The  three 


*  Fig  49. — Movements  of  a  particle  (»)  attached  to  the  surface  of  Amoeba  in 
passing  from  a  pseudopodium  at  the  posterior  end  over  the  body  to  a  pseudopo- 
dium at  the  anterior  end.     For  explanation  see  text. 


156  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

examples  above  given  are  typical  for  all.  They  show  the  following  as 
to  the  manner  in  which  the  pseudopodia  are  formed  when  they  are 
projected  freely  into  the  water. 

1.  The  pseudopodium  grows  in  length  chiefly  from  the  base,  so  that 
any  part  on  the  surface  retains  nearly  its  original  distance  from  the  tip. 

2.  The  increase  in  surface  as  the  pseudopodium  grows  is  not  pro- 
duced by  the  flowing  outward  and  backward  of  the  endosarc  at  the  tip 
with  its  transformation  into  ectosarc  (as  represented  by  Fig.  31),  but 
by  the  transference  of  a  portion  of  the  surface  layer  of  the  body  to  the 
pseudopodium.  The  same  substance  remains  at  the  tip  of  the  pseu- 
dopodium from  the  beginning  (observation  2,  p.  154  ;  I  have  other 
observations  showing  the  same  thing). 

3.  Thus  the  movement  of  the  free  pseudopodium  is  like  that  of  the 
pseudopodium  in  contact  with  a  surface,  save  that  in  the  latter  case  one 
side  is  held  back  by  attachment  to  the  substratum.  In  the  free  pseudo- 
podium all  sides  move  outward ;  in  the  attached  one,  all  sides  but  one. 

The  outer  layer  of  the  body  in  its  transference  to  the  pseudopodium 
may  doubtless  become  thicker  or  thinner  or  be  otherwise  modified.  As 
will  be  shown  later,  I  am  not  at  all  inclined  to  deny  the  possibility  of 
the  transformation  of  endosarc  into  ectosarc,  and  vice  versa.  The 
observations  show,  however,  that  this  transformation  of  substance  does 
not,  as  a  rule,  take  place  in  pseudopodia  by  means  of  the  "fountain 
currents"  represented  in  the  diagrams  from  Rhumbler  (Figs.  30-32). 

Further,  the  surface  of  the  pseudopodium  may  be  increased  by  the 
flowing  into  it  of  the  endosarc,  producing  a  sort  of  stretching  of  the 
outer  layer,  involving,  of  course,  the  appearance  at  the  surface  of  por- 
tions of  substance  which  were  before  covered. 

WITHDRAWAL   OF   PSEUDOPODIA. 

In  the  withdrawal  of  pseudopodia  the  process  is  the  reverse  of  that 
occurring  in  the  formation  of  pseudopodia,  as  is  shown  in  case  3,  above 
(p.  154,  Fig.  49).  The  basal  parts  of  the  pseudopodial  surface  first 
pass  on  to  the  body,  followed  by  the  distal  portions. 

The  withdrawal  of  pseudopodia  shows  certain  other  features  that  are 
of  importance  for  the  understanding  of  the  mechanism  of  amoeboid 
movement.  The  process  differs  somewhat  in  different  cases,  depending 
on  whether  the  withdrawal  is  slow  or  rapid.  When  the  pseudopodium  is 
slowly  withdiawn,  its  surface  may  remain  perfectly  smooth,  the  decrease 
in  surface  keeping  pace  with  the  decrease  in  volume,  until  the  pseudo- 
podium has  quite  disappeared.  But  when  the  withdrawal  is  more  rapid 
the  surface  becomes  thrown  into  folds  or  warty  prominences  of  various 
sorts.  This  is  more  common  than  retraction  without  the  formation  of 
such  prominences.      Evidently  the  volume  decreases  so  fast  that  the 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  1 57 

decrease  in  surface  cannot  keep  pace  with  it^  so  that  the  surface  is 
thrown  into  folds.  This  phenomenon  is  particularly  interesting  in  its 
bearing  on  the  theory  that  would  account  for  the  retraction  of  pseudo- 
podia  by  the  action  of  surface  tension.  On  this  theory  we  should 
naturally  expect  the  surface  to  remain  smooth,  and  by  no  means  to  be 
thrown  into  folds,  since  it  is  by  the  tendency  of  the  surface  to  decrease 
that  the  decrease  in  volume  is  accounted  for ;  the  decrease  in  volume 
should  not,  therefore,  precede  the  decrease  in  surface.  This  matter  will 
be  taken  up  later. 

As  the  pseudopodium  decreases  in  size,  the  fluid  endosarc,  of  course, 
flows  out  of  it  and  joins  the  endosarc  of  the  body.  The  backward 
current  begins  at  the  mouth  or  inner  end  of  the  pseudopodium,  and 
gradually  extends  backward  to  near  the  tip ;  the  current  is  most  rapid 
in  the  central  axis  of  the  pseudopodium,  and  in  this  axis  it  is  most 
rapid  at  the  inner  end.* 

Where  is  the  impelling  force  in  the  outflow  of  the  endosarc  and  the 
decrease  in  size  of  the  pseudopodium  }  The  observations  seem  to  sug- 
gest several  factors  here.  The  fact  that  the  ectosarc  of  the  pseudo- 
podium passes  on  to  the  body  when  the  pseudopodium  shortens,  as  is 
shown  in  Fig.  49,  a,  b^  c,  indicates  that  the  ectosarc  of  the  body  exercises 
a  pull  on  the  outer  layer  of  the  pseudopodium,  drawing  it  inward. 
This  would,  of  course,  force  the  fluid  endosarc  into  the  body.  But  this 
would  not  account  for  the  wrinkling  and  roughening  of  the  outer  surface 
of  the  pseudopodium,  which  is  so  prominent  a  feature  in  the  withdrawal. 
For  this  there  are  two  conceivable  causes,  (i)  The  ectosarc  itself  may 
contract  actively,  driving  out  the  endosarc.  If  the  real  contractile  por- 
tion of  the  ectosarc  is  not  on  the  outer  surface  (in  the  cuticula,  as  it  has 
sometimes  been  called),  but  in  a  deeper  layer,  then  the  outer  surface 
would  be  thrown  into  folds  or  prominences  as  contraction  occurs.  (2)  On 
the  other  hand,  it  is  conceivable  that  the  endorsarc  might  be  drawn  out 
of  the  pseudopodium,  the  latter  collapsing  and  becoming  wrinkled  as 
a  result.  This  is  the  explanation  given  by  Biitschli  (1893,  p.  201). 
This  view  would  have  to  assume  some  force  pulling  on  the  endosarc  at 
the  mouth  of  the  pseudopodium,  and  sufficient  viscosity  in  the  endosarc 
so  that  a  pull  thus  exercised  would  draw  out  the  whole  mass  contained 
within  the  pseudopodium.  Thus,  in  Fig.  49,  a,  the  general  advancing 
current  within  the  body  of  the  Amoeba  might  be  thought  to  exercise  a 
pull  at  the  point  j^  in  the  direction  of  the  arrow  ;  if  the  endosarc  were 


♦This  account  differs  from  that  given  by  Biitschli  (1880,  p,  116),  according  to 
whom  the  withdrawal  of  the  pseudopodium  begins  at  the  tip.  The  observations 
present  no  difficulty,  and  I  am  unable  to  understand  how  Biitschli  came  to  this 
result.  In  a  large  pseudopodium  the  method  of  retraction  described  above  is 
evident. 


158 


THE    BEHAVIOR    OF    LOWER    ORGANISMS. 


sufficiently  viscous  the  entire  mass  of  endosarc  would  be  withdrawn, 
and  the  pseudopodium  would  collapse. 

There  are  certain  facts  that  speak  against  this  second  view.  Thus, 
the  endosarc  often  passes  out  when  there  is  no  current  away  from  the 
mouth  of  the  pseudopodium,  so  that  there  can  be  nothing  pulling  upon 
the  endosarc.  A  pseudopodium  may  be  withdrawn  when  the  animal 
is  otherwise  quiet ;  or,  when  the  animal  is  stimulated  strongly,  all  the 
pseudopodia  may  be  withdrawn  at  the  same  time,  while  there  is  no 
endosarcal  current  in  the  body  of  the  animal.  A  striking  case  that 
belongs  here  is  sometimes  to  be  observed  in  Amceba  radiosa.  This 
animal  frequently  floats  in  the  water,  with  many  long,  pointed  pseudopo- 
dia radiating  in  all  directions  from  the  body.     Now,  if  the  pseudopodia 

are  stimulated  with  a  rod, 
they  begin  to  contract.  The 
endosarc  first  passes  inward, 
but  the  resistance  of  the  body 
is  so  great  that  the  fluid  stops 
at  the  base  of  the  pseudo- 
podia. These,  therefore, 
swell  up  in  a  bulbous 
fashion,  as  illustrated  in 
Fig.  50.  Such  cases,  indeed 
all  the  numerous  cases  in 
which  the  endosarc  passes 
out  of  a  pseudopodium  and 
comes  to  rest  as  soon  as  it  has 
left  the  latter,  can  only  be  ex- 
plained on  the  assumption 
that  the  endosarc  is  forced 
out  by  the  contraction  of  the  ectosarc,  or  by  some  active  movements  of 
the  endosarc  itself,  of  a  character  not  understood. 

Further,  there  are  certain  facts  which  speak  positively  in  favor  of 
the  view  that  the  production  of  the  wrinkles  is  due  to  a  contraction  of  the 
inner  layer  of  the  ectosarc.  Thus,  when  an  Amoeba  is  strongly  stimu- 
lated and  withdraws  all  its  pseudopodia  quickly,  the  whole  surface  of 
the  body  becomes  rough  and  wrinkled.  The  endosarc  has  not  passed 
out  of  it,  so  that  it  cannot  be  considered  in  a  state  of  collapse  ;  on  the  con- 
trary, it  is  clearly  contracted  as  strongly  as  possible.  Again,  if  a  large 
pseudopodium  is  cut  from  the  body,  it  contracts  strongly,  showing  the 
rough,  wrinkled  contour,  though  the  endosarc  has  not  passed  out  of  it. 


Fig.  50.* 


♦Fig.  50. — Specimen  oi Amoeba  radiosa  in  which  the  endosarc  has  passed  out 
of  the  distal  portions  of  the  pseudopodia  into  the  basal  parts,  causing  them  to 
swell  up  in  .1  bulbous  fashion. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


159 


The  processes  occurring  in  a  retracting  pseudopodium  are  the  same 
as  those  taking  place  at  the  posterior  end  in  a  moving  animal.  In  fact, 
the  cases  are  really  identical ;  the  posterior  portion  of  the  body  may  be 
considered  merely  a  large  retracting  pseudopodium.  Often,  as  we  shall 
see,  it  is  impossible,  from  its  method  of  formation,  to  consider  it  any- 
thing else. 

The  pseudopodia  are,  of  course,  usually  formed  in  the  anterior  part 
of  the  Amoeba,  in  contact  with  the  substratum,  and  are  directed  in  the 
line  of  progression,  or 
at  a  slight  angle  with 
the  line  of  progression. 
As  they  are  withdrawn, 
their  surface,  as  we  have 
seen,  usually  becomes 
folded  or  roughened, 
and  the  small  roughened 
projection  resulting 
from  the  withdrawal 
lasts,  as  a  rule,  for  a  long 
time.  As  the  Amoeba 
continues  its  forward 
course,  the  base  of  the 
retracting  pseudopo- 
dium retains  nearly  its 
original  position,  as  do 
the  other  parts  of  that 
layer  of  the  ectosarc  that 
is  against  the  substra- 
tum, so  that  the  body 
of  the  Amoeba  gradually 
passes  the  pseudopo- 
dium, and  the  latter 
finally  becomes  united  with  the  posterior  end.  During  this  transference  to 
the  rear,  the  pseudopodium  usually  changes  its  position  (Fig.  51 ).  At 
first  it  is  directed  nearly  forward  («),  then  it  takes  a  position  at  right 
angles  to  the  body  (^),  and  finally  swings  around  with  its  point  directed 


Fig.  5 


♦Fig.  51. — Successive  stages  in  the  retraction  of  a  pseudopodium.  At  a  the 
pseudopodium  extends  forward  at  the  anterior  edge  ;  at  3  it  has  partly  withdrawn 
and  stands  at  right  angles  to  the  body,  which  has  partly  passed  it;  at  c  the 
pseudopodium  is  directed  backward,  and  is  in  the  posterior  part  of  the  body;  at 
</the  small  roughened  remnant  of  the  pseudopodium  has  nearly  united  with  the 
tail.  At  X  the  successive  positions  occupied  by  the  withdrawing  pseudopodium 
are  shown  in  a  single  diagram. 


|6o  THE    BEHAVIOR    OF   LOWER   ORGANISMS. 

nearly  backward  (Fig.  51,  c).  This  change  of  position  is  due  to  the 
contraction  of  the  posterior  part  of  the  Amoeba.  The  ectosarc  just 
behind  the  base  of  the  pseudopodium  contracts  toward  the  middle,  as 
described  on  page  171.  As  a  result  the  pseudopodium  must  swing 
around  till  it  points  nearly  backward.  The  mechanism  of  the  process 
will  be  best  understood  by  an  examination  of  Fig.  51,  at. 

Finally,  what  remains  of  the  pseudopodium  reaches  the  posterior 
end  or  tail  (Fig.  51,  d).  By  this  time  usually  all  that  is  left  of  it  is  a 
small  roughened  projection,  its  surface  being  of  essentially  the  same 
character  as  that  of  the  tail.  This  projection  fuses  completely  with  the 
tail,  its  projections  taking  up  a  portion  of  the  surface  of  the  latter.  The 
tail  is  in  fact  nothing  but  the  fused  remnants  of  all  the  pseudopodia 
that  have  been  formed,  together  with  the  contracted  outer  layer  of  the 
body  of  the  Amoeba  (the  latter  cannot  be  distinguished  in  any  essential 
way  from  a  pseudopodium).  A  roughened  tail  is  formed  de  novo  when- 
ever an  Amoeba  suddenly  changes  its  direction  of  movement.  The 
previous  anterior  end  then  becomes  roughened  in  contracting  and  forms 
a  typical  tail.  This  latter  unites  with  the  old  tail  if  any  of  the  latter 
remains.  The  substance  of  the  tail  gradually  passes  forward  into  the 
rest  of  the  body,  as  we  have  seen. 

MOVEMENTS    AT    THE    ANTERIOR    EDGE. 

As  in  Amceba  verrucosa  and  its  relatives,  so  in  the  species  of  more 
changeable  form,  the  most  active  movements  are  taking  place  at  the 
anterior  edge.  In  Amceba  proteus  ?ind  A.  Umax  one  sees  still  more 
distinctly  than  in  the  species  before  named  the  pushing  forward  of  a 
series  of  waves  of  hyaloplasm  which  become  attached  to  the  substratum 
in  front.  In  Amceba  Umax  and  its  relatives  especially  such  a  wave 
may  be  very  pronounced,  extending  forward  at  times  one-fifth  the 
length  of  the  body  or  more,  though  usually  much  less. 

At  first  the  advancing  wave,  as  it  moves  rapidly  forward,  is  usually 
free  from  granules,  and  may  be  spoken  of,  therefore,  as  hyaloplasm. 
If  the  motion  is  less  rapid,  however,  it  contains  granules,  and  is  not 
distinguishable  in  any  way  from  the  interior  endosarc.  Where  it  is  at 
first  free  from  granules,  it  is  nevertheless  highly  fluid  in  character,  as 
is  shown  by  the  fact  that  it  flows  and  spreads  out  swiftly,  and  that  the 
granules  of  the  endosarc  pass  into  it  rapidly.  The  freedom  of  the 
advancing  hyaloplasm  from  granules  is  not  due  to  its  greater  density 
or  solidity  as  a  result  of  the  action  of  water  upon  it,  as  has  sometimes 
been  maintained,  for  it  is  at  first  free  from  granules ;  then,  after  the 
water  has  acted  longer  upon  it,  it  becomes  filled.  Apparently  the 
reason  for  its  freedom  from  granules  is  merely  the  fact  that  it  moves 
forward  faster  than  the  granules  and  leaves  them  behind.     This  view 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


l6l 


is  supported  by  the  variations  to  be  observed  in  the  relation  of  the  clear 
substance  to  the  granular  substance  at  the  anterior  end.  These  varia- 
tions arise  chiefly  from  the  different  rates  of  movement  of  the  two 
substances,  and  may  be  summarized  as  follows : 

I .  The  clear  substance  moves  fastest  at  first,  and  therefore  becomes 
separated  from  the  granules  as  a  broad  band  in  front  (Fig.  52,  a);  this 
is  then  immediately  filled  completely  by  the  granules.  Even  large 
granules  or  vacuoles  pass  to  the  very  anterior  edge,  so  that  one  sees 
but  a  line  between  these  and  the  quter  water. 


Fig.  52.* 

2.  The  clear  substance  advances  fastest,  and  so  continues  to  do,  so  that 
it  remains  a  long  time  as  a  broad,  clear  band  in  front  of  the  granules. 

3.  The  two  substances  advance  at  the  same  rate,  so  that  there  is  no 
separation  between  them.    The  granules  and  vacuoles  are  then  found  at 


♦  Fig.  52. — Distribution  of  hyaloplasm  and  granules  at  the  anterior  end  in 
Amoeba  Umax  and  its  relatives  :  a,  hyaloplasm  without  granules  at  the  anterior 
end ;  b,  granules  and  vacuole  at  the  anterior  edge ;  c  and  d,  two  successive 
instants  in  the  locomotion ;  at  c  the  anterior  half  of  the  body  is  free  from  gran- 
ules, the  latter  being  heaped  up  behind  a  well-marked  barrier;  at  d  the  barrier 
has  burst  at  a  certain  point  (a;),  allowing  a  stream  of  granules  to  flow  forward  to 
the  anterior  edge;  e  andy,  two  successive  stages  at  the  advancing  anterior  end; 
in  e  the  clear  hyaloplasm  has  stopped  at  the  line  x-y\  at/"  the  hyaloplasm  has 
advanced,  while  the  granules  are  heaped  up  behind  the  same  line  x-y. 


l62  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  advancing  edge.  This  condition  is  not  at  all  rare.  In  such  cases 
there  is  at  the  anterior  end  less  clear  space  between  the  granular  region 
and  the  water  than  in  any  other  part  of  the  body.  In  fact,  there  is 
typically  no  space  at  all.  I  have  seen  large  vacuoles  come  so  close  to 
the  anterior  edge  at  such  times  that  it  was  not  possible  to  distinguish 
between  the  boundary  of  the  vacuole  and  the  boundary  of  the  Amoeba 
(Fig.  52,  <5). 

4.  Finally,  either  hyaloplasm  or  endosarc  or  both  may  stop  in  any 
of  the  positions  mentioned  above.  Thus  the  hyaloplasm  may  stop, 
whereupon  the  endosarc  flows  into  it  and  fills  it,  or  both  may  stop,  so 
that  the  hyaloplasm  remains  empty,  as  a  clear  band,  for  a  long  time. 

The  line  separating  hyaloplasm  and  endosarc  is  at  times  very  sharply 
defined,  as  has  often  been  pointed  out.  A  number  of  unusually  favorable 
specimens  gave  me  the  opportunity  of  determining  the  reason  for  this, 
in  many  cases  at  least.  The  Amoeba  in  question  (Fig.  52,  c-f)  was  an 
elongated,  rapidly  moving  form,  much  resembling  A,  limax^  but  having 
usually  two  contractile  vacuoles,  one  very  large,  in  the  fore  part  of  the 
body,  the  other  smaller  and  in  the  rear.  The  body  contained  many 
fine  granules,  which,  when  the  animal  was  at  rest,  were  scattered  almost 
uniformly  through  the  body;  the  peripheral,  more  solid  zone  (usually 
called  ectosarc)  contained  as  many  of  these  as  did  the  endosarc. 

In  moving  this  Amoeba  usually  sends  out  first  a  large  amount  of  clear 
fluid  containing  no  granules  ;  this  at  times  extends  so  far  as  to  constitute 
half  the  length  of  the  Amoeba  (Fig.  52,  c).  There  is  a  perfectly  sharp 
line  between  the  clear  hyaloplasm  and  the  granular  endosarc,  and  behind 
this  line  the  granules  of  the  endosarc  are  heaped  up,  as  if  under  pressure. 
Suddenly  this  line  gives  way  over  a  small  area  (at  x)^  and  the  granules 
pour  through  it  in  a  thin  stream  nearly  or  quite  to  the  anterior  tip  of 
the  Amoeba  (Fig.  52,  d).*  Gradually  the  whole  barrier  gives  way,  and 
nothing  is  left  to  .mark  the  position  it  occupied.  If  after  its  first  out- 
flow the  hyaloplasm  has  stopped,  the  whole  Amoeba  is  filled  with 
granules.  But  if,  as  is  usually  the  case,  after  a  pause  the  hyaloplasm 
has  started  forward  again,  the  granules  of  the  endosarc  stream  forward 
not  to  the  anterior  tip,  but  only  to  the  line  which  formed  the  anterior 
boundary  of  the  hyaloplasm  at  its  pause  {x-y^  Fig.  52,  e^f).  Here 
the  granules  stop  and  are  heaped  up  again,  until  finally  the  barrier 
breaks  as  before,  and  the  granules  rush  forward  again,  to  be  stopped 
at  a  new  line. 

The  explanation  of  these  phenomena  becomes  evident  on  careful 
examination.  It  is  to  be  noted  that  the  line  x-y  which  stops  the 
flow  of  the  granules  of  endosarc  is  always  identical  with  one  which 


*  Similar  phenomena  have  been  observed  by  Prowazek  (1900,  p.  17 ;  Fig.  18). 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  1 63 

formed  the  anterior  boundary  of  the  hyaloplasm  (that  is,  of  the  Amoeba 
as  a  whole)  at  a  previous  pause.  The  reason  for  this  is  as  follows : 
The  lower  surface  of  the  Amoeba,  as  we  know,  is  at  rest ;  here  the 
protoplasm  has  become  modified  to  form  a  sort  of  membrane.  This 
membrane  extends  up  a  very  little  distance  at  the  sides  and  ends  (as 
is  shown  by  the  fact  that  the  protoplasm  at  the  sides  is  at  rest).  Thus 
at  the  anterior  end  there  is,  after  a  pause,  a  low  barrier  formed  by  this 
membrane.  The  next  wave  of  advancing  hyaloplasm  arises  just  behind 
this  barrier,  overleaps  it,  and  pushes  forward  (the  conditions  being 
essentially  the  same  as  in  Amoeba  verrucosa^  already  described).  This 
advancing  wave  when  first  formed  is  very  thin,  forming  a  mere  sheet 
lying  on  the  substratum.  This  is  shown  by  the  fact  that  when  the  out- 
line of  the  remainder  of  the  Amoeba  is  sharply  in  focus,  the  anterior 
portion  is  often  undefined,  and  one  is  compelled  to  focus  lower  to  get 
its  outline  sharply.  The  thin  sheet  of  hyaloplasm  which  has  just  pushed 
forward  is  bounded  behind  by  a  low  wall,  formed  from  the  membrane 
which  previously  limit- 
ed it  in  front  (Fig.  53, 
x).  Now  the  granules 
of  the  endosarc  flow  for- 
ward until  they  reach 
this  boundary ;  there 
they  stop  and  become 
heaped  up  against  it  (Fig.  53).  After  a  time  the  membrane  forming 
this  barrier,  since  it  is  now  completely  enveloped  by  protoplasm,  be- 
comes dissolved  and  gives  way  in  the  manner  described  above ;  the 
granules  then  flow  forward.  Meanwhile,  a  new  partial  boundary 
has  been  left  in  front  by  the  hyaloplasm  ;  this  again  stops  the  endosarc, 
and  the  whole  process  is  repeated  many  times. 

Of  course,  when  the  anterior  boundary  advances  uniformly,  without 
pauses,  no  anterior  membrane  is  formed,  and  there  is  nothing  to  hold 
back  the  granules  of  the  endosarc  ;  hence  there  is  no  reason  for  a  separa- 
tion of  hyaloplasm  and  endosarc,  and  we  find  that  none  exists.  On  the 
other  hand,  when  the  Amoeba  has  paused  for  a  long  time  the  anterior 

*  Fig.  53.-— Diagram  of  a  longitudinal  section  of  the  anterior  edge  of  Amoeba, 
to  show  the  cause  of  the  stopping  of  the  granules  of  the  endosarc  some  distance 
behind  the  anterior  margin.  The  line  beneath  represents  the  substratum  to 
which  the  Amoeba  is  attached.  The  anterior  h_yaloplasm  at  first  moves  forward  to 
the  line  x-x ;  stopping  there  it  becomes  covered  with  a  firmer  wall,  as  represented 
by  the  heavy  black  line.  Now  the  hyaloplasm  pushes  forward  from  above  the 
anterior  edge  x-x,  forming  a  thin  sheet  closely  applied  to  the  substratum,  as 
shown  in  the  figure.  The  endosarcal  granules  flow  forward,  but  are  stopped  by 
the  barrier  x-x  (the  former  anterior  boundary  of  the  Amoeba) ;  they  cannot  flow 
forward  till  this  boundary  is  liquefied. 


164  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

membrane  seems  especially  well  developed,  for  the  hyaloplasm  pushes 
then  a  long  way  ahead  and  may  form  half  the  length  of  the  Amoeba 
before  the  endosarc  has  burst  through  the  membrane. 

The  phenomena  described  above  are  very  general  in  creeping  Amoebae, 
both  in  those  with  usually  but  a  single  pseudopodium  (as  A.  Umax), 
and  in  those  with  many  pseudopodia  (as  A.  angulata). 

Of  course,  the  general  fact  that  there  is  a  separation  between  hyalo- 
plasm and  endosarc  is  not  explained  by  these  observations ;  thus  we 
know  that  they  are  often  separated  even  in  pseudopodia  that  are  pro- 
jected freely  into  the  water.  But  the  phenomena  are  much  less  marked 
in  such  cases ;  it  is  exactly  the  observed  difference  between  them  and 
the  phenomena  to  be  seen  in  a  creeping  Amoeba  that  the  above  obser- 
vations explain. 

In  all  these  details  it  is  important  not  to  lose  sight  of  the  essential 
point  in  the  movement  at  the  anterior  end.  This  is  as  follows  :  The  new 
wave  begins  on  the  upper  surface  just  behind  the  former  boundary  line, 
and  rolls  forward,  so  that  its  former  upper  surface  is  now  in  contact 
with  the  substratum. 

This  method  of  movement  explains  a  peculiar  fact  which  one  observes 
frequently,  and  which  I  found  it  difficult  to  understand  before  this 
movement  was  demonstrated.  The  advancing  edge  in  Amoeba  usually 
does  not  push  forward  fine,  loose  particles  lying  on  the  substratum  in 
front  of  it,  but  overlaps  them  instead,  so  that  the  Amoeba  creeps  over 
them.  This  is  especially  noticeable  when  the  water  contains  many 
particles  of  India  ink  or  of  soot.  In  view  of  the  rolling  movement  with 
the  series  of  waves,  each  coming  from  behind  the  previous  anterior 
edge  and  thus  descending  on  the  substratum  from  above,  this  burying 
of  loose  movable  particles  becomes  intelligible. 

In  Amoeba  proteus  and  its  relatives  the  advancing  anterior  edge  does 
not  move  forward  in  a  single  uniform  curve,  as  it  does  in  A.  verru- 
cosa, and,  as  a  rule,  in  A.  Umax.  On  the  contrary,  the  anterior  edge 
may  show  the  most  varied  form  and  modeling  (Fig.  54)  ;  narrow  points 
may  be  sent  out  here  ;  a  broad  rounded  lobe  there  ;  a  rectangular  projec- 
tion elsewhere.  Pseudopodia  may  rise  above  the  general  level,  pro- 
jecting freely  into  the  water  and  later  coming  in  contact  with  the 
substratum,  or  be  withdrawn  without  coming  thus  in  contact.  The 
anterior  portion  of  the  body  may  divide  into  two  lobes,  or  may  become 
hollowed  out  so  as  to  contain  a  cavity  bounded  by  thin  walls  (see 
later.  Figs.  ^^,  76).  These  facts  show  clearly  that  the  method  of 
advance  of  the  anterior  edge  cannot  possibly  be  determined  by  general 
pressure  from  behind,  such  as  would  be  produced,  for  example,  by  a 
contraction  of  the  posterior  part  of  the  body.  Such  pressure  could  not 
produce  the  cavity  shown  in  Fig.  75  or  the  thin  edge  bearing  numerous 
points  shown  in  Fig.  54. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


•65 


MOVEMENTS    OF   THE    POSTERIOR    PART    OF   THE    BODY. 

In  an  Amoeba  moving  as  a  simple,  elongated  mass,  the  anterior  por- 
tion of  the  body  is  broadest  and  very  thin,  being  flattened  against  the 
substratum,  while  the  posterior  part  is  narrower  and  much  thicker.  In 
many  cases  the  posterior  end  rises  to  an  actual  hump,  the  body  being 
thickest  at  the  posterior  edge,  or  a  little  in  front  of  this  edge  (Figs.  44, 
58).  This  is  true  as  well  of  the  Amoebae  of  nearly  constant  form  (A. 
verrucosa^  etc..  Fig.  44),  as  of 
those  related  to  A,  proteus.  From 
this  hump  the  upper  surface  slopes 
forward  to  the  thin  anterior  edge. 
The  margins  in  the  posterior  part  of 
the  body  are  not  thin,  but  rounded 
like  the  surface  of  a  cylinder. 

The  anterior  portion  of  the 
Amoeba  is  attached  to  the  substra- 
tum. This  attachment  of  the  ante- 
rior portion  has  been  clearly  demon- 
strated by  Rhumbler  (1898),  and  I 
can  confirm  his  results  throughout. f 
The  attachment  is  probably  by  a 
mucus-like  secretion  ;  at  least  such 
a  secretion  exists,  as  Rhumbler  and 

others  have  shown  and  I  can  confirm.  I  have  sometimes  been  able  to 
pull  an  Amoeba  about  by  using  a  glass  rod  to  which  a  thread  of  this 
mucus  had  become  attached  (Fig.  55).  The  animal  then  seems  to 
follow  the  rod  at  a  distance,  the  thread  of  mucus  not  being  visible. 
In  virtue  of  this  attachment  the  Amoeba  resists  currents  of  water, 
or  the  impinging  of  solid  bodies  against  it.  The  posterior  portion 
of  the  body  is  not  thus  attached,  but  is  entirely  free  from  the  bottom. 

In  many  cases  the  most  posterior  part  of  the  body  forms  a  more  or 
less  distinctly  marked  oflT  portion,  the  surface  of  which  is  wrinkled  or 
warty  or  villous,  or  otherwise  irregular.  This  is  variously  known  as 
the  tail,  the  villous  patch,  or  appendage  (Wallich,  Leidy),  houppe 
(Penard),  Schopf  (Rhumbler),  etc.  The  occurrence  of  this  appendage 
is  variable.  In  some  species  it  is  usually  present,  in  others  less  com- 
mon. Its  occurrence  and  degree  of  development  vary,  indeed,  in  the 
same  individual. 


Fig.  54. 


♦Fig.  54. — Amoeba  angulata  in  locomotion,  showing  the  numerous  points  in 
the  anterior  region,  some  attached  to  the  substratum,  others  projecting  freely  into 
the  water,     a  is  the  "antenna-like"  pseudopodium,  described  on  p.  177. 

tit  is  rather  curious  that  Biitschli  (1892),  in  his  discussion  of  the  movements 
of  Amoeba,  is  inclined  to  deny  that  there  is  any  attachment  to  the  substratum. 


1 66  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

In  an  advancing  Amoeba  the  posterior  end  moves  forward  at  about 
the  same  rate  as  does  the  anterior,  since  the  distance  between  the  two 
remains  about  the  same.  Leaving  out  of  account  for  the  moment 
specimens  with  the  wrinkled  appendage,  there  is  a  continual  current 
forward  from  the  posterior  end.  Nevertheless,  the  latter  remains  on 
the  average  of  about  the  same  size.     The  material  which  flows  out  of 

it  above  is  supplied  from 
beneath.  As  we  have 
seen,  a  layer  of  material 
at  the  under  surface  of 
the  Amoeba  is  at  rest. 
The  main  portion  of  the 
body  passes  over  this 
layer,  dragging  the  pos- 
^^^'  ^^*  terior  end.     The   latter 

takes  up  as  it  passes  the  resting  layer  which  was  against  the 
substratum.  This  gradually  becomes  fluid,  and  passes  for- 
ward again  in  the  advancing  current.  All  this  may  be 
clearly  seen  by  observing  the  course  of  individual  particles 
in  the  protoplasm  and  on  the  surface,  and  is  fully  set 
forth  in  the  preceding  pages  of  this  paper. 

The  unattached  posterior  portion  steadily  contracts  as  it 
moves  forward.  Particles  on  its  upper  surface  are  moving  forward,  as 
we  have  seen  in  detail.  But  this  is  not  all.  Particles  on  its  sides  and 
under  surface  likewise  move  forward ;  there  is  an  actual  contraction 
independent  of  the  streaming  already  described.  The  movement  of 
substance  due  to  this  contraction  is  more  striking  and  rapid  as  we 
approach  the  posterior  end.  As  this  contraction  is  an  important  fact, 
it  will  be  well  to  give  some  details  of  the  observations  which  show  it 
to  exist. 

Particles  attached  to  the  lower  surface,  or  to  the  lateral  margins  of 
the  Amoeba,  next  to  the  substratum,  in  the  anterior  part  of  the  body, 
remain  quiet  for  a  long  time.  But  this  lasts  only  till  they  have  reached 
that  portion  of  the  body  which  is  free  from  the  substratum  ;  then  they 
begin  to  move  slowly  forward  as  a  result  of  the  contraction  just 
described.  Of  two  such  objects,  one  nearer  the  posterior  end,  the 
hinder  one  moves  the  more  rapidly,  so  that  the  distance  between  the 
two  slowly  but  distinctly  decreases.  Though  such  objects  on  the  bot- 
tom or  sides  move  forward,  they  do  so  less  rapidly  than  does  the 
posterior  end.  The  latter,  therefore,  in  time  overtakes  them,  and  they 
are  finally  pulled  around  the  posterior  end  to  the  upper  surface,  where 
they  pass  forward,  as  we  have  already  seen  in  detail. 

*  Fig.  55. — An  Amoeba  drawn  backward  by  a  thread  of  its  viscid  secretion. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


167 


Fig.  56.* 


The  contraction  of  the  posterior  part  of  the  body  is  further  shown  by 
the  behavior  of  retracted  pseudopodia.  When  a  pseudopodium  con- 
tracts it  usually  produces,  as  we  have  seen,  a 
small  wart-like  excrescence,  which  persists 
for  some  time.  Such  wart-like  remains  of 
pseudopodia  behave  like  foreign  bodies  at- 
tached to  the  margin  of  the  Amoeba.  In  the 
anterior  half  they  remain  quiet,  while  in  the 
free  posterior  half  they  move  slowly  forward, 
as  a  result  of  the  contraction  of  this  part  of 
the  body.  When  two  or  more  of  these  rem- 
nants of  pseudopodia  are  formed  at  once, 
with  an  interval  between  them,  this  interval 
becomes  less  as  a  result  of  the  more  rapid 
movement  of  the  hinder  one. 

The  contraction  of  this  posterior  region  is 
sometimes  very  striking,  especially  when  the 
posterior  end  becomes  attached  to  some  for- 
eign object  and  is  drawn  out  longer  than 
usual ;  when  it  finally  becomes  free  it  con- 
tracts suddenly  and  rapidly.  Thus,  for  example,  an  Amoeba  hav- 
ing the  form  shown  in  Fig.  56,  a^  began  to  move  in  the  direction 
shown  by  the  arrow,  when  it  became  evident  that  the  posterior  end  was 
attached  to  a  diatom  shell,  which  was  fast  to  the  substratum.  As  the 
Amoeba  crept  away  the  posterior  end  was  drawn  out,  as  shown  at  b. 
Finally  the  diatom  became  detached  from  the  bottom,  when  the  stretched 
posterior  end  at  once  contracted,  shortening  up  rapidly,  so  that  the 
Amoeba  had  the  form  shown  at  c.     Such  observations  are  often  made. 

This  contraction  does  not  occur  in  that  part  of  the  Amoeba  which  is 
attached  to  the  bottom,  but  begins  at  once  as  soon  as  the  attachment 
ceases.  One  might  compare  the  outer  layer  to  a  stretched  sheet  of  India 
rubber  that  is  attached  to  a  surface  by  means  of  some  adhesive  sub- 
stance. As  soon  as  the  adhesion  gives  way  the  sheet  contracts.  There 
is  no  definite  point  at  which  the  attachment  to  the  substratum  must 
cease  ;  sometimes  it  is  farther  forward,  sometimes  farther  back.  The 
gradual  freeing  of  the  posterior  portion  can  be  clearly  observed  in  many 
cases,  particularly  in  Amoeba  a7igulata^  and  may  be  seen  to  go  hand 
in  hand  with  the  contraction  of  the  ectosarc.  As  soon  as  a  certain  part 
of  the  body  becomes  free,  its  contraction  takes  place  with  some  sudden- 
ness, and  the  contraction  is  the  more  noticeable  the  greater  the  part  of 
the  body  that  is  freed  at  once.     Often  the  process  of  becoming  freed 

*FiG.  56. — Successive  forms  of  an  Amoeba,  showing  the  marked  contraction 
of  the  posterior  end.     (See  text). 


l68  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

takes  place  in  a  series  of  jerks,  and  there  is  a  corresponding  jerkiness 
in  the  contractions  of  the  posterior  part  of  the  body.  When  a  large 
amount  of  surface  is  freed  at  once  there  is  a  sudden  forward  rush  of  the 
fluid  portion  of  the  Amoeba,  with  a  striking  contraction  of  the  posterior 
part  of  the  body.  Such  a  case  as  is  shown  in  Fig.  56  is  only  an  unusu- 
ally strong  contraction  of  this  sort,  due  to  the  fact  that  the  hinder  part 
on  the  body  had  remained  locally  attached  longer  than  usual. 

As  a  result  of  this  contraction,  the  ectosarc  of  the  posterior  part  of 
the  body  becomes  thickened  and  wrinkled,  or  warty.  The  change  from 
a  flat  plate  to  a  rounded  form  involves  a  decrease  in  the  amount  of  exter- 
nal surface,  and  as  the  amount  of  material  in  the  surface  layer  is  not  at 
once  decreased,  this  layer  is  compelled  to  fold  and  become  wrinkled  and 
warty.  When  this  process  is  very  pronounced  we  have  produced  at 
the  posterior  end  the  wrinkled,  warty  appendage  so  often  described. 
Such  a  roughened  structure  may  be  produced  in  any  part  of  the  Amoeba 
by  rapid  contraction,  as  we  have  seen  above  (p.  160).  The  rough, 
warty  appendage  at  the  posterior  end  is  the  common  product  of  all  the 
contractions  which  have  taken  place. 

In  Amoeba  verrucosa  and  its  relatives  the  current  forward  on  the  upper 
surface  extends  backward  to  the  posterior  end  ;  the  outer  surface  of  the 
latter  seems  not  markedly  different  in  texture  from  that  of  the  rest  of 
the  body.  In  other  species  of  Amoeba  there  is  a  greater  difference 
between  the  texture  of  the  surface  layer  of  the  anterior  part  of  the  body 
and  that  of  the  posterior  end,  and  this  may  involve  some  differences  in 
the  movements.  Often,  in  even  these  species,  the  forward  current 
extends  backward  to  the  very  posterior  end  ;  particles  on  the  under  side 
pass  up  over  the  posterior  end  and  forward,  just  as  in  A.  verrucosa 
(see  p.  147).  But  in  other  cases,  in  A.  lt?nax^  A.  froteus^  etc.,  the 
surface  material  at  the  posterior  end  is  so  stiffened  that  it  is  temporarily 
excluded  from  the  current.  There  is  then  produced  the  distinct,  rough- 
ened appendage,  which  is  for  a  time  dragged  passively  behind  the 
Amoeba.  In  such  a  case  the  currents  from  beneath  pass  upward  on 
either  side  of  this  appendage,  meeting  in  the  middle  line  (Fig.  57). 
Particles  attached  to  the  under  surface  on  either  side  of  the  appendage, 
therefore,  soon  pass  to  the  upper  surface  and  are  carried  forward,  while 
those  on  the  under  surface  of  the  appendage  itself  may  remain  in  position 
and  be  dragged  forward  for  a  considerable  time. 

But  I  have  rarely  found  this  posterior  appendage  so  completely  cut 
off' from  the  general  circulation  as  is  often  supposed.  Usually  there  is 
a  very  slow  current  forward  on  the  upper  surface  of  the  appendage, 
involving  also  its  internal  parts.  Into  this  current  particles  attached 
to  the  posterior  end,  and  even  to  the  under  surface  of  the  appendage, 
are  in  course  of  time  drawn.    I  have  thus  seen  particles  of  soot  dragged 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  169 

about  for  ten  minutes  at  the  posterior  end,  then  finally  pass  upward  into 
the  surface  current,  where  they  were  carried  to  the  anterior  end.  Even 
when  this  slow  current  from  the  posterior  appendage  is  completely 
suspended  the  suspension  is  only  temporary.  The  currents  after  a  period 
begin  again,  and  a  strongly  marked  warty  posterior  appendage  may  in 
time  completely  disappear,  its  substance  hav- 
ing become  mingled  with  that  of  the  remain- 
der of  the  Amoeba. 

Other  parts  of  the  Amoeba  may  become 
temporarily  immobile  and  thus  excluded  from 
the  general  circulation.    One  often  sees  certain  Fig.  57.* 

parts  of  Amoeba  proteus  and  other  similar  species  thus  quiet,  while  the 
restof  thebod3MS  in  active  motion  (see  Rhumbler,  1S98,  o.  122). 

In  the  species  with  "eruptive"  pseudo  podia  this  process  seems  to 
have  gone  farthest.  Here  the  whole  outer  layer  apparently  becomes 
hardened  at  times,  so  that  movement  occurs  only  when  the  inner  sub- 
stance bursts  through  this,  forming  "eruptive"  pseudopodia.  In  this 
case  the  pseudopodia  formation  apparently  differs  from  that  in  Amoeba 
proteus  and  its  relatives,  as  described  above,  in  the  fact  that  the  ectosarc 
of  the  body  is  not  transferred  to  the  surface  of  the  pseudopodium.  I 
have  not  been  able  to  study  this  process  in  detail  further  than  to  deter- 
mine that  there  is  no  backward  current  on  such  pseudopodia.  The 
matter  is  worthy  of  further  examination.  In  Amoeba  verrucosa^  the 
species  which  has  been  hitherto  supposed  to  have  the  most  immobile 
ectosarc,  we  have  shown  that  the  outer  layer  is  in  continual  rotary 
motion  in  the  progressing  animal. 

GENERAL  VIEW  OF  THE  MOVEMENTS  OF  AMCEBA  IN  LOCOMOTION. 

Let  us  now,  with  the  aid  of  a  diagram,  attempt  to  form  a  clear  con- 
ception of  the  movements  occurring  in  an  Amoeba  that  is  progressing 
in  a  definite  direction,  with  a  view  to  determining  the  nature  of  the 
forces  at  work.  Fig.  58  may  represent  a  longitudinal  section  of  such 
an  Amoeba  as  seen  in  a  side  view.  The  anterior  end,  A^  is,  as  we  have 
seen,  very  thin,  and  is  applied  closely  to  the  substratum,  while  the 
posterior  end,  P^  is  high  and  rounded,  forming  a  sort  of  pouch.  It  is 
free  from  the  substratum,  beginning  at  the  point  at,  at  about  the  middle 
of  the  body. 

At  the  anterior  end  waves  of  hyaloplasm  are  pushed  forward  one 
after  the  other,  so  that  the  anterior  end  successively  occupies  the  posi- 
tions «,  ^,  c.  As  we  know,  it  is  the  upper  surface  which  thus  pushes 
out ;  it  rolls  over,  so  that  a  point  which  was  originally  on  the  upper 


♦Fig.  57. — Diagram  of  the  surface  currents  when  the  posterior  appendage  is 
excluded  from  the  general  stream. 


ifjO  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

surface  becomes  applied  to  the  substratum.  It  is  evident  that  the  sur- 
face of  the  Amoeba  is  increased  in  extent  by  the  pushing  out  of  these 
waves. 

On  the  upper  surface  of  the  Amoeba  there  is  a  forward  current  of  the 
outer  layer,  as  indicated  by  the  arrows.  This  current  extends  back- 
ward to  the  posterior  end,  where  it  is  continued  as  a  movement  upward 
from  the  lower  surface.  This  upward  movement  stops,  at  any  given 
movement,  at  about  the  point  jj/,  though,  of  course,  the  point  where 
it  ceases  cannot  be  precisely  fixed.  That  part  of  the  lower  surface 
which  is  in  contact  with  the  substratum,  from  the  anterior  end  to  x^  is 
quiet.  That  part  of  the  lower  surface  which  is  not  in  contact  with  the 
substratum  (from  x  to  y)  is  moving  slightly  forward  owing  to  the  con- 
traction in  this  region,  as  described  on  pages  166-168.  This  movement 
is  comparatively  slight,  as  indicated  by  the  small  arrows.     Within  the 


Jtr      JC'  a    o   c 

Fig.  58.* 

Amoeba  are  currents  moving  forward  in  the  same  direction  as  the 
current  on  the  upper  surface. 

The  posterior  end  as  a  whole  moves  forward,  so  that  it  comes  to 
occupy  later  the  position  shown  by  the  dotted  line.  The  point  x^ 
where  the  lower  surface  of  the  Amoeba  becomes  free  from  the  sub- 
stratum, moves  forward  an  equivalent  amount  to  x.  The  entire 
Amoeba  thus  moves  forward  in  the  direction  indicated  by  the  large 
arrow  above. 

Thus  far  our  account  has  been  purely  descriptive,  containing  only 
what  has  been  demonstrated  by  observation  and  experiment,  and  intro- 
ducing nothing  hypothetical.  We  must  now  endeavor  to  form  a  con- 
ception of  the  location  and  direction  of  action  of  the  forces  at  work  In 
producing  the  movements.  Discussion  of  the  ultimate  character  of 
the  forces  will  be  reserved  for  the  section  on  the  theories  of  amoeboid 
movement. 

One  of  the  primary  phenomena  is  evidently  the  pushing  forward  of 

♦Fig.  58. — Diagram  of  the  movements  of  Amoeba,  as  seen  in  side  view.  A^ 
anterior  end;  P,  posterior  end;  a,  b,  c,  successive  positions  occupied  by  the  an- 
terior edge.  The  large  arrow  above  shows  the  direction  of  locomotion ;  the 
other  arrows  show  the  direction  of  the  protoplasmic  currents,  the  longer  arrows 
indicating  the  more  rapid  currents.     For  further  explanation  see  text. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I7I 

the  anterior  edge.  The  form  of  the  Amoeba  shows  that  this  cannot  be 
due  to  pressure  from  behind,  for  if  the  pressure  were  greatest  behind 
and  less  in  front,  the  mass  of  internal  fluid  would,  of  course,  be  forced 
forward,  and  the  Amoeba  would  be  thickest  in  front  instead  of  behind ; 
the  form  of  anterior  and  posterior  ends  would  be  reversed.  In  the 
varied  modeling  of  the  anterior  end  we  have  seen  another  proof  of  the 
impossibility  of  accounting  for  the  action  here  by  pressure  from  behind 
(p.  164).  Further,  the  forward  current  on  the  upper  surface  of  the 
Amoeba  could  not  possibly  be  produced  by  pressure  from  behind. 
The  impossibility  of  accounting  for  the  form  and  movement  by  pres- 
sure from  behind  has  been  recognized  by  most  investigators,  though 
on  other  grounds  than  those  here  set  forth. 

On  the  other  hand,  if  we  take  the  view  that  the  anterior  wave,  after 
attaching  itself  to  the  substratum,  exercises  a  pull  on  the  parts  behind 
it,  the  rest  of  the  phenomena  follow  most  naturally.  Such  a  pull 
would  draw  forward  the  tenacious  upper  layer  of  the  body,  and  we 
find  that  this  is  actually  moving  forward.  The  mass  of  inactive  inter- 
nal contents  would  drag  behind  as  far  as  possible,  so  that  the  thickest 
part  of  the  Amoeba  would  be  at  the  rear,  and  this  is  exactly  what  we 
find  to  be  true.  The  posterior  end  would  be  dragged  forward.  This, 
also,  is  true.  In  its  movement  forward  it  would  be  partly  rolled  ;  that 
is,  its  lower  surface  would  gradually  pass  upward  and  become  the  upper 
surface.  This,  also,  we  know  to  be  true.*  Finally,  the  internal  fluid 
contents  would  be  compelled  to  stream  forward  as  the  anterior  end 
advanced  and  the  posterior  end  followed  it.  This  streaming  is,  of 
course,  one  of  the  striking  features  of  the  Amoeba.  The  character- 
istics of  the  endosarcal  streaming  are,  I  believe,  exactly  what  might 
be  expected  from  the  method  of  origin  just  set  forth. 

We  have  one  other  more  or  less  independent  factor  of  the  movement 
in  the  contraction  of  the  posterior  part  of  the  body  that  is  not  in  con- 
tact with  the  substratum.  As  we  have  seen,  the  substance  of  the  sides 
and  bottom,  as  well  as  of  the  upper  surface,  are  moving  forward  in 
this  region,  as  indicated  by  the  small  arrows  of  the  diagram  (between 
;vandjv).  Moreover,  we  know  that  there  is  a  lateral  contraction  as 
well  as  an  antero-posterior  one,  for  the  wide,  flat  anterior  portion 
shrinks  together  as  soon  as  it  is  released  from  the  substratum.  This 
contraction  should  probably  be  brought  into  relation  with  the  previous 
increase  of  surface  at  the  anterior  end.  As  the  anterior  wave  is  sent 
forth  the  surface  at  the  anterior  end  is  much  increased.  We  might  com- 
pare the  action  with  the  stretching  of  a  sheet  of  India  rubber.  This 
tense  portion  then  becomes  attached  to  the  substratum,  as  we  might 

*  Large  bodies  within  the  Amoeba  close  against  the  posterior  surface  are  often 
rolled  over  in  this  process,  as  I  have  several  times  observed. 


172  THE   BEHAVIOR   OF   LOWER    ORGANISMS. 

fasten  the  stretched  sheet  of  India  rubber  by  means  of  a  strong  cement 
to  a  plate  of  glass.  Upon  being  released  the  tense  layer  of  protoplasm 
contracts  again,  just  as  the  rubber  sheet  would  do.  In  the  protoplasm 
the  contraction  takes  place  rather  slowly,  causing  the  steady  pulling 
forward  of  the  posterior  half  of  the  body,  as  exhibited  by  objects  attached 
to  its  lower  surface. 

In  connection  with  the  contraction  of  the  lower  surface  as  just  de- 
scribed we  must  consider  also  certain  properties  of  the  upper  surface. 
When  this  is  pulled  upon  by  the  advancing  anterior  wave  it  does  not 
respond  like  an  inelastic  membrane,  but  like  an  elastic,  contractile  one. 
If  it  were  inelastic  its  motion  would  follow  that  of  the  anterior  end 
exactly,  and  thus  take  place  in  a  series  of  jerks.  But  this  does  not 
occur.  When  the  anterior  wave  pushes  forward,  thus  extending  the 
upper  surface,  there  is  no  immediate  increase  in  the  movement  of  this 
surface,  nor  of  the  posterior  end ;  the  movement  forward  is  a  steady 
one.  The  property  of  contractility  is  further  shown  very  directly  in  the 
phenomena  which  take  place  when  a  large  portion  of  the  lower  surface 
of  the  Amoeba  is  suddenly  released,  as  described  on  page  167.  It  seems 
clear  that  the  entire  surface  of  the  Amoeba  is  in  a  state  of  tension  and  that 
this  tension  is  directed  toward  the  advancing  anterior  end.  The  condi- 
tion would  be  imitated  by  partly  filling  a  rubber  sack  with  a  heavy  fluid, 
causing  one  surface  to  adhere  to  the  substratum  and  pulling  on  one  side. 

As  a  result  of  this  tension  on  the  surface  the  internal  contents  of  the 
Amoeba  must,  of  course,  be  under  a  certain  slight  amount  of  pressure. 
As  we  have  seen  (p.  171)  even  without  this  pressure  the  internal  con- 
tents must  flow  forward,  since  the  posterior  surface,  against  which 
they  are  resting,  is  moved  forward.  But  the  pressure  accounts  for 
certain  details  of  the  movements  of  the  endosarc.  Thus,  when  a  pseudo- 
podium  is  sent  forth,  or  one  of  the  anterior  waves  moves  forward,  it  is 
usually  soon  filled  by  endosarc.  In  its  pushing  forward  the  pseudo- 
podium  forms  a  region  where  the  tension  is  relieved  ;  the  fluid  contents, 
under  pressure  elsewhere,  therefore  flow  into  it. 

It  is  to  be  noted  that  this  pressure  is  a  mere  consequence  of  the  tension 
due  to  the  pushing  forward  of  the  anterior  edge,  and  is  by  no  means  a 
cause  of  the  pushing  forward  ;  it  is  always,  therefore,  subordinate  to  and 
dependent  upon  the  latter,  and  is  not  a  matter  of  primary  significance. 

Altogether,  then,  our  results  lead  us  to  look  upon  Amoeba  as  an  elastic 
and  contractile  sac,  containing  fluid.  In  locomotion  one  side  of  this  sac 
actively  stretches  out,  becomes  attached  to  the  substratum,  and  draws 
the  remainder  of  the  sac  after  it  in  a  rolling  movement.  The  primary 
phenomena  are  the  stretching  out  of  one  side,  the  elasticity,  and  the 
contractility  of  the  outer  layer. 

Whether  this  elasticity  and  contractility  should  not  be  considered 


THE    MOVEMENTS   AND    REACTIONS    OF    AMCEBA.  1 73 

properties,  not  merely  of  the  outer  layer,  but  of  the  entire  substance  of 
the  Amoeba,  may  be  a  question.  The  fact  that  ectosarc  and  endosarc 
are  mutually  interconvertible  would  seem  to  imply  an  affirmative  answer 
to  this  question,  and  I  believe  other  evidence  could  be  adduced  looking 
in  the  same  direction.  But  the  locomotion  itself  seems  to  require  these 
properties  only  in  the  ectosarc,  so  that  we  shall  for  the  present  leave  out 
of  consideration  the  question  as  to  their  existence  in  the  endosarc. 

To  the  three  primary  phenomena  above  mentioned  we  must  devote 
further  attention.  It  has  been  maintained  by  certain  writers  that  the 
ectosarc  is  not  an  elastic  and  contractile  membrane,  as  above  set  forth ; 
hence  we  must  examine  the  evidence  on  that  point.  There  then  remain 
the  questions  :  What  is  the  cause  of  the  pushing  out  at  the  anterior  edge  ? 
and.  What  is  the  essential  nature  of  the  contractility  of  the  ectosarc? 
These  questions  will  be  reserved  for  a  special  section  on  the  theories 
of  amoeboid  movement.  We  will  at  this  point  investigate  certain 
general  properties  of  the  substance  of  Amoeba,  with  a  view  espe- 
cially to  determining  whether  we  are  justified  in  considering  the 
ectosarc  elastic  and  contractile,  though  not  limiting  our  attention  to 
these  properties  alone. 

SOME  CHARACTERISTICS  OF  THE  SUBSTANCE  OF  AMCEBA. 
FLUIDITY. 

It  is,  of  course,  not  necessary  to  dwell  upon  this  point ;  it  has  been 
treated  in  detail  recently  by  Rhumbler  (1898,  1902)  and  Jensen  (1900). 
For  anyone  who  is  familiar  with  the  movements  of  Amoeba  from  per- 
sonal observation,  doubt  cannot  exist  that  its  protoplasm  has  at  least 
some  of  the  most  striking  properties  of  fluids,  notably  the  property  of 
flowing,  with  the  freedom  of  movement  of  the  particles  with  reference  to 
each  other  that  this  implies.  This  applies  most  strongly  to  the  endosarc  ; 
for  the  ectosarc,  as  we  shall  see,  there  are  decided  limitations  to  the 
fluidity.  Nevertheless,  the  particles  of  the  ectosarc  have,  to  a  considera- 
ble degree,  that  freedom  of  movement  with  relation  to  each  other  that  is 
characteristic  of  fluids.  This  is  shown,  for  example,  by  the  fact  that  any 
portion  of  the  ectosarc  may  be  temporarily  excluded  from  the  advanc- 
ing stream  (especially  common  at  the  posterior  end,  p.  169),  and  in  the 
fact  that  neighboring  portions  of  the  ectosarc  may  flow  in  opposite 
directions  (p.  148).  But  the  characteristics  of  the  ectosarc  are  much 
more  those  of  a  tough,  rather  persistent  skin  than  has  sometimes  been 
supposed.     This  point  is  brought  out  in  the  following  sections. 

rhumblkr's  "  knto-ectoplasm  process." 
The  movements  of  the  outer  layer  of  the  body  described  in  this  paper 
have  an  important  bearing  on  the  transformation  of  endosarc  into  ecto- 
sarc and  vice  versa^  of  which  so  much  is  said  in  Rhumbler's  recent 


174  "^"^    BEHAVIOR    OF    LOWER    ORGANISMS. 

extensive  paper  (1898).  My  observations  show  that  this  transforma- 
tion is  confined  within  much  narrower  limits  than  Rhumbler  supposed. 
In  the  account  which  he  gives  of  the  movements  of  Amoeba  this  trans- 
formation (the  "  ento-ectoplasm  process,"  as  he  calls  it)  plays  a  very 
large  part,  and  is  essential  to  locomotion.  At  the  anterior  end,  accord- 
ing to  Rhumbler,  endosarc  constantly  flows  out  to  the  surface  and  is 
there  transformed  into  ectosarc,  flowing  back  as  such  along  the  surface 
of  the  body.  Somewhere  in  the  posterior  part  of  the  body  or  at  the  base 
of  a  pseudopodium  this  ectosarc  passes  inward  and  is  retransformed 
into  endosarc.  These  supposed  processes  are  indicated  in  the  diagrams 
from  Rhumbler,  Figs.  30-33. 

My  observations  show  that  this  view  of  the  constant  inter-transforma- 
tion of  the  two  layers  is  incorrect,  and  that  we  must  attribute  to  the 
ectosarc  a  much  higher  degree  of  permanence  than  Rhumbler  supposed. 
There  is  no  regular  transformation  of  endosarc  into  ectosarc  at  the 
anterior  end.  On  the  contrary,  the  ectosarc  here  retains  its  continuity 
unbroken,  moving  across  the  anterior  end  in  the  same  manner  as  across 
other  parts  of  the  body.  In  the  same  way,  the  ectosarc  is  not  regularly 
transformed  into  endosarc  in  the  hinder  part  of  the  body.  We  can  trace 
a  single  definite  point  on  the  ectosarc  (or  a  complex  of  such  points 
having  a  definite  relation  to  each  other)  continually  until  it  has  passed 
completely  around  the  Amoeba ;  several  complete  rotations  of  this  sort 
are  described  from  actual  observation  on  page  141 .  In  the  species  having 
very  changeable  forms  a  single  point  on  the  ectosarc  may  be  traced, 
for  example,  from  the  surface  of  a  pseudopodium  at  the  posterior  end 
across  the  whole  length  of  the  body  to  near  the  tip  of  a  long  pseudo- 
podium at  the  anterior  end  (Fig.  49,  p.  155) ;  there  is  no  reason  to 
suppose  that  it  could  not  be  traced  indefinitely  but  for  the  difficulties 
of  observation. 

On  the  other  hand,  there  is  no  doubt  that  ectosarc  may  be  trans- 
formed into  endosarc,  and  vice  versa^  under  certain  conditions.  This 
process  was  apparently  first  clearly  seen  by  Wallich  (1863,  a,  p.  370). 
Wallich  saw  the  formation  of  "  eruptive  pseudopodia  "  by  the  outflow 
of  the  endosarc  through  a  small  perforation  in  the  ectosarc.  A  portion 
of  the  latter  was  thus  covered  by  the  endosarc,  and  gradually  resorbed. 
Rhumbler  figures  a  similar  case  (1898,  p.  152),  and  I  have  repeatedly 
seen  such.  Further,  as  Rhumbler  has  shown,  and  as  I  can  confirm,  in 
A.  verrucosa  food  bodies  are  enclosed  in  a  layer  of  thick  ectosarc,  which 
passes  with  the  food  into  the  endosarc,  there  to  be  resorbed  (seep.  195). 

Thus,  it  is  clear  that  there  may  be  a  transformation  of  one  layer  into 
the  other  under  special  circumstances,  but  such  transformation  is  much 
less  general  than  Rhumbler  supposed,  and  is  by  no  means  a  regular 
accompaniment  of  locomotion. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  1 75 

ELASTICITY   OF    FORM    IN    AMCEBA. 

For  a  real  understanding  of  the  phenomena  shown  by  amoeboid 
protoplasm  it  is  important  to  realize  that  it  has,  besides  some  of  the 
chief  characteristics  of  fluids,  a  number  of  properties  that  are  usually 
considered  characteristic  of  solids.  This  came  out  clearly  in  certain 
of  my  experiments.  They  show  that  Amoeba  has  elasticity  of  form  to 
a  considerable  degree. 

These  experiments  consisted  in  changing  the  shapes  of  Amoebae  with 
a  fine  capillary  glass  rod,  under  the  microscope,  in  the  open  drop. 
From  numerous  experiments  of  this  character  the  following  may  be 
selected  as  typical : 

An  Amoeba  had  sent  out  one  rather  long,  thick  pseudopodium,  as 
shown  in  Fig.  59,  a.  With  the  capillary  glass  rod  this  pseudopodium, 
a^  was  pulled  loose  from  the  bottom  and  bent  over  into  the  position 
shown  by  the  dotted  outline  b.     On  being  released  it  rather  quickly 


Fig.  6o.t 

sprang  back  into  its  original  position,  a.  This  experiment  was  repeated 
on  different  Amoebae  many  times. 

An  elongated  Amoeba  («-«,  Fig.  60)  was  bent  with  the  rod  at  about 
its  middle,  so  that  the  anterior  half  was  pushed  far  to  one  side  of  the 
original  median  axis  (to  b).  This  anterior  half  at  once  attached  itself 
to  the  bottom,  whereupon  the  posterior  half,  which  was  not  attached, 
immediately  swung  round  into  line  with  it,  so  that  the  Amoeba  occu- 
pied the  position  b-c.  Thus  the  original  straight  Amoeba  on  being 
bent  immediately  straightens  itself  out  again.  On  repeating  this  experi- 
ment with  many  elongated  individuals  it  was  found  that  frequently  the 
straightening  out  was  not  quite  complete,  so  that  after  it  had  occurred 
there  was  still  a  slight  bend  in  the  middle. 

An  Amoeba  had  a  long  pseudopodium  curved  over  to  one  side,  as  in 
Fig.  61,  a.     This  pseudopodium  was  loosened  from  the  bottom  with 


♦Fig.  59. — A  straight  pseudopodium,  a,  is  bent  into  the  position  b  with  a  rod. 
It  at  once  returns  to  the  position  a. 

tFiG.  60. — A  narrow  Amoeba,  a-a,  is  bent  with  the  rod  into  the  position  a-b  , 
the  end,  b,  then  becomes  attached,  and  the  animal  at  once  straightens  into  the 
position  b-c. 


176  THE   BEHAVIOR    OF   LOWER    ORGANISMS- 

the  rod  and  straightened  out  {b) .     On  being  released  it  at  once  swung 
back  to  its  original  form  and  position  at  a. 

An  Amoeba  had  many  long,  slender,  free  pseudopodia  standing  out 
radially  from  the  body.  These  could  be  pushed  repeatedly  to  one  side 
or  the  other,  or  bent  at  a  marked  angle.  In  every  case  they  returned 
at  once  to  the  radial  position. 

An  indefinite  number  of  such  experiments  could  be  detailed.     They 

show  clearly  that  Amoeba  has,  to  a  certain  degree  at  least,  one  of  the 

most  distinctive  properties  of  solids,  a  tendency  to  resist  deformation  of 

shape,  and  to  restore  the  shape  when  changed.     It  will  be  observed 

that  the  cases  are  not  such  as  can  be  accounted  for  on  the  assumption 

that  Amoeba  is  a  simple  fluid  mass  which  tends  to  take  a  certain  form 

in  accordance  with  the  principle  of  least  surfaces.     A  small  sphere  of 

fluid  when  deformed  returns  to  its  original  shape  in  conformity  with 

the  principle  just  mentioned.     But  such  returns  to  the  original  form  as 

^-^^^  ^  are  illustrated  in  Fig.  59 

(       \  and  Fig.  61,  for  example, 

y^^      '"'^'      N.     \      \  are  not  required   by  the 

Q^  1        A  principle  of  least  surfaces 

\^^  V^ /.— . . ,- s^      so  long  as  the  Amoeba  is 

^^^^^^^  J  J  ^  considered  a  simple  fluid 

-— ^"^'^  mass. 

^''^-  ^'•*  On   the  other  hand,  if 

we  consider  Amoeba  not  as  a  simple  fluid,  but  as  a  fluid  mass  of 
a  foamlike  or  alveolar  structure,  composed  of  a  tense  meshwoik  of  one 
fluid  enclosing  minute  drops  of  another,  then  the  results  above  set 
forth  might  be  explained  without  assuming  that  the  protoplasm  has 
in  any  part  passed  from  a  liquid  to  a  solid  state.  This  follows 
from  th^  considerations  and  experiments  recently  set  forth  by  Rhum- 
bler  in  a  most  important  and  suggestive  paper  (1902).  Rhumbler 
shows  that  a  fluid  mass  having  alveolar  structure  must  react  to  tran- 
sient pressure  from  without  like  an  elastic  body  ;  in  other  words, 
that  it  must  have  elasticity  of  form.  The  results  which  I  have  set 
forth  above  might  almost  seem,  then,  to  have  been  predicted  in  Rhum- 
bler's  summing  up:  "Transient  tensions  or  pressures  produce  an 
elastic  reaction  of  the  cell  body;  longer  action,  on  the  other  hand, 
produces  a  plastic  reaction  "  (/.  <:.,  p.  371).  For  the  detailed  demonstra- 
tion of  this  principle  the  reader  must  be  referred  to  the  original  paper 
of  Rhumbler.  It  will  suffice  to  note  here  that  the  result  is  due  to  the 
fact  that  deformations  of  the  body  as  a  whole  produce  deformations  of 
the  alveoli,  and  that  the  surface  tension  of  the  alveolar  walls  tends  to 

*  Fig.  61. — A  large,  curved  pseudopodium,  a,  is  straightened  out  into  the  posi- 
tion b  with  a  rod.     On  being  released  it  at  once  returns  to  the  position  a. 


THE    MOVEMENTS   AND    REACTIONS    OF   AMCEBA.  1 77 

restore  them  at  once  to  their  original  form,  resulting  in  a  return  of  the 
whole  body  to  its  original  form. 

If,  then,  we  hold  that  the  substance  of  Amoeba  is  composed  of  such 
an  alveolar  structure,  the  above  observations  are  intelligible,  even 
though  no  part  of  the  substance  of  the  organism  is  in  the  solid  state. 
But  whatever  the  cause,  we  must  recognize  that  the  protoplasm  of 
Amoeba  shows  in  the  gross  some  of  the  characteristics  of  solids. 

Leaving  out  of  account  the  minute  structure  of  the  protoplasm,  most 
or  all  of  the  observations  detailed  above  could  be  accounted  for  on  the 
assumption  that  the  body  of  Amoeba  consists  of  a  sac  of  fluid,  the  outer 
wall  of  the  sac  being  tough  and  elastic,  and,  as  is  shown  later,  contrac- 
tile. In  this  case  only  the  outer  layer,  the  ectosarc,  would  show  the 
characteristics  of  matter  in  the  solid  state  of  aggregation.  Certain 
observations  made  by  the  writer  indicate  that  this  is  the  true  state  of  the 
case.  These  observations  are  as  follows  :  In  several  cases  a  long,  slender 
pseudopodium,  formed  of  both  endosarc  and  ectosarc,  was  stimulated  at 
the  tip,  causing  the  endosarc  to  be  withdrawn,  and  leaving  the  pseudo- 
podium formed  of  ectosarc  alone,  as  illustrated  in  Fig.  50,  page  158.  Such 
pseudopodia  could  with  the  glass  rod  be  bent  sharply  at  an  angle,  and 
would  often  remain  thus  for  some  time.  If,  while  thus  sharply  bent, 
the  endosarc,  as  sometimes  happens,  begins  to  flow  back  into  the 
pseudopodium,  the  latter  straightens  out  with  a  sort  of  jerk  as  soon  as 
the  endosarc  begins  to  fill  it.  The  ectosarc  thus  acts  like  an  empty 
glove-finger,  which  might  bend  over  when  empty  but  which  would 
straighten  out  on  becoming  filled  with  a  fluid.  A  tough  skin  could 
perhaps  be  formed  by  an  alveolar  fluid  in  accordance  with  the  princi- 
ples developed  by  Rhumbler  as  above  set  forth.  Whatever  the  explana- 
tion, the  experiments  indicate  the  existence  of  this  tough  skin-like  layer 
on  the  outer  surface  of  the  body. 

CONTRACTILITY    IN   THE    ECTOSARC   OF   AMCEBA. 

Besides  elasticity  of  form,  the  outer  layer  of  Amoeba  clearly  has  the 
power  of  contracting  locally.  This  is  a  fact  which  is  omitted  from 
consideration  in  many  of  the  theories  in  which  amoeboid  movement  is 
referred  to  local  changes  in  the  surface  tension  of  a  fluid  mass.  It  will 
be  well,  therefore,  to  set  forth  some  of  the  observations  on  this  point. 
I  transcribe  here  some  of  my  notes,  with  the  corresponding  sketches. 

1.  Specimen  with  a  single  long,  prominent,  curved  pseudopodium. 
This  rather  quickly  swings  around  bodily  toward  its  concave  side,  and 
unites  with  the  protoplasm  of  the  body  (Fig.  62,  a). 

2.  A  specimen  sends  out  a  long,  curved  pseudopodium  (Fig.  62,  6), 
This  slowly  straightens  out,  passing  from  position  i  to  position  2. 

3.  A.  angulata  usually  sends  out  at  the  anterior  end  a  single 
pointed  pseudopodium  obliquely  upward  into  the  water  (Fig.  62,  c). 
This  point  frequently  waves  from  side  to  side  like  an  antenna. 


178 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


4.  An  Amceba  was  creeping  on  the  surface  film,  with  a  very  long, 
slender  pseudopodium  trailing  behind  down  into  the  water  and  bent  to 
one  side.    This  pseudopodium  suddenly  swung  far  over  to  the  other  side. 

5.  Amoeba  with  many  pseudopodia  extending  in  all  directions  freely 
into  the  water.  Just  as  withdrawal  begins,  a  given  pseudopodium 
bends  over  to  one  side,  becomes  curved  to  form  a  half  circle,  or  waves 
back  and  forth  from  one  side  to  the  other. 

An  indefinite  number  of  such  observations  could  be  adduced,  showing 
that  with  its  other  movements  Amceba  has  the  power  of  bending  and 

straightening  its  pseudopodia  and  waving 
them  from  side  to  side.  Such  movements 
have,  of  course,  been  described  by  many 
authors ;  in  the  magnificent  monograph  of 
the  Rhizopoda  by  Penard  (1902)  many 
still  more  striking  cases  than  those  I  have 
described  are  set  forth.  Some  of  them 
should  be  quoted.  In  Amozba  radiosa  the 
pseudopodia  "  maybe  displaced  as  a  whole 
in  the  liquid,  and  I  have  seen  them  de- 
scribe in  this  manner  a  quarter  of  a  full 
circle  in  a  second,  like  the  handsof  a  watch 
which  one  pushes  forward  suddenly  by  fif- 
teen minutes.  On  two  or  three  occasions 
also  I  have  noticed  in  the  very  sharp  point 
of  a  pseudopodium  a  rapid  movement  of 
wave-like  vibration,  so  that  one  could  com- 
pare itwithaflagellum"  (/.<:.,p.88).  Simi- 
lar phenomena  are  described  for  Amoeba 
Umax  (p.  36),  A.  gorgonia  (p.  79),  and 
especially  for  A.  ambulacralis  (pp.  91 ,  92), 
in  which  the  pseudopodia  act  like  tentacles. 
In  other  rhizopods,  relatives  of  Amoeba, 
Penard  describes  similar  phenomena.  Thus 
in  Pamfhagus  mutabilis  (p.  439)  the  pseudopodia  are  said  to  move 
as  a  whole  in  the  water  "almost  as  quickly  as  flagella."  Similar 
facts  are  described  for  Difflugia  fristis  (p.  255),  Cystodifflugia  sac- 
cuius  (p.  429),  Pamphagus  granulatus  (p.  436),  Nadinella  tenella 
(p.  462),  and  various  other  rhizopods.    Penard  compares  the  movements 


Fig.  62.* 


♦  Fig.  62. — Movements  of  pseudopodia :  a,  a  pseudopodium  in  the  position  i 
bends  quickly  in  the  direction  shown  by  the  arrow,  and  unites  with  the  body; 
*,  a  curved  pseudopodium,  i,  straightens  into  the  position  2;  c,  the  antenna-like 
anterior  pseudopodium  of  ./l/«ce3«  angulata;  it  vibrates  from  I  to  2,  thence  back 
through  I  to  3,  etc. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  l^g 

of  the  pseiidopodia  in  many  cases  to  the  vibrations  of  flagella.  Similar 
movements  of  pseudopodia  have,  of  course,  been  described  by  other 
authors,  including  Biitschli  (1878,  p.  272;  1880,  p.  123).  The  strik- 
ing resemblance  of  the  movements  of  the  pseudopodia  in  some  cases  to 
those  of  flagella  (see  especially  the  account  of  Podostoma,  Clapar^de  & 
Lachmann,  1858,  p.  441)  seems  to  indicate  that  the  motion  in  these 
two  classes  of  structures  must  be  essentially  similar  in  character,  and 
that  no  theory  of  amoeboid  movement  is  likely  to  be  correct  that  is 
inconsistent  with  the  movements  offlagella.  Certain  suggestions  as  to 
the  possibility  of  bringing  the  two  in  relation  are  given  in  the  theoretical 
portion  of  the  present  paper  (p.  218). 

The  whole  body  is  sometimes  moved  rapidly  by  such  movements  of 
the  pseudopodia.  This  happens  especially  when  the  body  is  suspended 
in  the  water  and  bears  many  long  pseudopodia,  one  of  which  comes 
in  contact  with  the  substratum.  This  pseudopodium  spreads  out  and 
extends  along  the  surface  for  a  distance,  the  part  along  the  surface 
forming  nearly  a  right  angle  with  the  free  portion.  Suddenly  the 
pseudopodium  straightens ;  since  the  distal  end  is  attached,  the  body 
is  thrown  almost  violently  against  the  substratum. 

Somewhat  similar  movements  take  place  frequently  in  Amoe6a  ver- 
rucosa and  its  relatives,  without  the  formation  of  pseudopodia.  The 
course  of  events  is  usually  as  follows :  A  specimen  is  creeping  in  a 
certain  direction  in  the  usual  manner  with  the  anterior  border  attached, 
while  the  posterior  end  is  raised  a  slight  distance  from  the  substratum. 
As  a  reaction  to  stimulus,  or  for  some  other  reason,  the  anterior  end 
releases  itself  from  the  bottom.  The  posterior  end  thereupon  sinks 
down  and  becomes  attached.  Then  its  ectosarc  contracts  slightly,  in 
such  a  way  as  to  lift  the  anterior  end  suddenly.  The  animal  thus  stands 
upon  what  was  its  posterior  end.  Now,  by  varied  contractions  of  the 
parts  of  the  ectosarc  in  contact  with  the  substratum,  the  animal  may 
jerk  from  side  to  side  rapidly  and  repeatedly,  reminding  one  of  the 
movements  of  certain  caterpillars  which  jerk  their  anterior  ends  about 
in  a  similar  manner.  These  movements  are  very  striking  and  are  much 
more  rapid  than  any  that  occur  in  other  species  of  Amoeba,  so  far  as 
I  have  observed. 

The  animal  may  even  move  from  place  to  place  in  this  manner. 
Standing  on  one  end,  it  jerks  its  body  suddenly  over  to  one  side,  so  that 
the  previously  upper  end  comes  close  to  the  substratum.  This  end  now 
becomes  attached,  while  the  other  is  released.  Next  a  new  sudden  con- 
traction brings  the  released  end  upward,  so  that  the  animal  now  occupies 
a  new  location,  one  body's  length  from  that  previously  occupied.  I  have 
never  seen  the  movement  go  any  farther  than  what  I  have  just  described, 
so  that  there  is  no  evidence  that  this  method  is  employed  for  bringing 
about  orderly  locomotion. 


i8o 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


These  movements  remind  one  of  the  "  rolling  motion  "  described  by 
Rhumbler(i898,  p.  115)  for  these  species,  though  they  take  place  with- 
out any  noticeable  change  of  form  and  in  a  manner  entirely  different 
from  the  movements  described  by  Rhumbler.  As  we  have  seen  above 
(p.  140),  the  normal  locomotion  of  these  species  is,  in  a  certain  sense, 
of  a  "  rolling"  character,  so  that  the  phenomena  described  by  Rhumb- 
ler as  the  rolling  movements,  perhaps  really  presented  nothing  different 
in  principle  from  the  usual  motion,  though  occurring  in  a  different  way 
because  the  organism  was  unattached. 

In  addition  to  movements  of  the  character  above  described,  certain 
other  phenomena  show  in  a  different  way  the  contractility  of  the  ecto- 
sarc.  Thus,  I  stimulated  sharply  with  a  glass  rod  one  side  of  an  elon- 
gated moving  specimen  of  Amoeba 
Umax  about  one-third  its  length  from 
the  posterior  end  (Fig.  63,  a).  The 
body  at  once  contracted  rapidly,  in  a 
ring-like  manner  (3),  at  this  point, 
J  and  in  about  \\  seconds  the  posterior 
portion  was  cut  off  completely,  save 
by  a  fine  thread  (c),  by  which  it 
hung  to  the  anterior  portion  for  a 
minute  or  two.  Later  this  broke, 
and  the  posterior  piece  finally  under- 
went degeneration. 

Penard,  in  his  great  work  on  the 
Rhizopoda,  describes  similar  phe- 
nomena in  Amoeba  terricola  {ver- 
rucosa^ after  injury  to  the  ectosarc. 
After  a  small  injury  the  injured  region  is  invaginated,  forming  a  small 
tube  passing  inward,  which  is  later  resorbed.  But  if  the  injury  is  large 
the  part  surrounding  it  contracts  strongly,  forming  a  deep  constriction 
between  it  and  the  remainder  of  the  body  (Fig.  64),  and  this  injured 
portion  is  finally  constricted  off  completely  (Penard,  1902,  p.  109).! 

Altogether,  then,  we  may  consider  it  thoroughly  demonstrated  that 
the  ectosarc  has  the  power  of  contracting  in  definitely  limited  regions 
in  such  a  way  as  (i)  to  produce  movements  of  entire  pseudopodia  com- 
parable to  those  of  flagella  ;  (2)  to  produce  ringlike  contractions  which 
may  even  progress  so  far  as  to  cut  the  body  in  two  completely. 

We  need  not,  therefore,  hesitate  to  admit  the  existence  of  contrac- 
tions of  the  ectosarc  in  ordinary  locomotion ;  these  are,  for  the  rest, 
as  clearly  observed  as  those  just  described. 

*  Fig.  63. — An  A.  Umax  is  stimulated  strongly  near  the  posterior  end  at  a;  the 
stimulated  part  thereupon  constricts  (*,  c),  separating  off  the  posterior  end  (rf). 
t  For  other  observations  on  reactions  to  injuries  see  pp.  202-204. 


Fig.  63.^ 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  l8l 

REACTIONS  TO  STIMULI. 

Of  particular  importance  for  the  understanding  of  the  behavior  of 
organisms  are  those  reactions  which  determine  the  direction  of  locomo- 
tion. Experiments  show  that  the  stimuli  to  such  reactions  must,  in  a 
slow-moving  organism  like  Amoeba,  affect  only  one  side  of  the  body, 
or  at  least  affect  different  parts  of  the  body  differently.  Owing  to  the 
minute  size  of  Amoeba,  it  is  difficult  to  apply  stimuli  in  such  a  way  as 
to  fulfill  this  condition.  Heat  or  cold,  or  a  chemical  in  solution,  for 
examples,  when  applied  to  one  side  are  likely 
to  extend  to  the  other  side,  and  far  beyond, 
before  the  slow  reaction  of  Amoeba  has  taken 
place  ;  the  reaction  when  it  occurs  is  then  to  a 

general,  and  not  to  a  local    stimulation.      For  „ 

.  .  Fig.  64.* 

this  reason  the  reactions    of   Amoeba    to    such 

general  stimulation  are  much  better  known  than  those  to  stimuli  locally 

applied.     I  have  devoted  myself  to  the  reactions  to  localized  stimuli, 

and  have  succeeded  in  overcoming  the  experimental  difficulties  for  a 

number  of  different  classes  of  agents,  though  not  for  all. 

In  examining  the  reactions  to  stimuli,  it  will  be  necessary  to  keep  in 
mind  the  method  of  locomotion  (set  forth  briefly  on  p.  169  ;  diagram 
in  Fig.  58,  p.  170) .  The  factors  to  which  special  attention  must  be  paid 
are  :  (i)  the  sending  out  (or  rolling  over,  as  perhaps  it  would  be  better 
to  say)  of  waves  of  the  ectosarc  on  one  side,  determining  the  anterior 
end  in  the  locomotion  ;  (2)  the  attachment  to  the  substratum  ;  (3)  the 
contraction  of  parts  of  the  body. 

The  reactions  were  studied  chiefly  in  Amoeba  proteus  and  A.  angu- 
lata;  where  other  species  were  used,  they  are  specifically  mentioned. 

REACTIONS    TO    MECHANICAL    STIMULI. 

The  reaction  to  mechanical  stimuli  may  be  either  positive  or  negative. 

POSITIVE    REACTION. 

An  Amoeba  floating  in  the  water  frequently  takes  a  starlike  form, 
with  many  long  pseudopodia  projecting  in  all  directions.  If  one  of 
these  pseudopodia  comes  in  contact  with  a  solid  object  or  the  surface 
film  (which  may  always  be  considered  a  solid  for  these  purposes) ,  the 
portion  in  contact  flattens  out,  attaches  itself  to  the  object,  and  its  proto- 
plasm begins  to  flow  out  in  a  sheet  over  the  latter.  The  other  pseudo- 
podia are  now  slowly  withdrawn  and  the  entire  animal  spreads  out  on 
the  solid,  moving  usually  in  the  direction  inaugurated  by  the  first 
pseudopodium  which  came  in  contact.  Often  in  passing  to  the  surface 
of  the  solid  there  are  a  number  of  rapid  jerking  movements,  due  to 


*  Fig.  64. — A.  verrucosa  constricting  ofFan  injured  region,  after  Penard  (1902). 


l82 


THE   BEHAVIOR    OF    LOWER   ORGANISMS. 


Straightening  out  or  bending  of  pseudopodia  as  described  on  p.  179. 
After  becoming  completely  transferred  to  the  surface  of  the  solid  the 
form  may  differ  much  from  that  of  the  floating  Amoeba.  Fig.  65  illus- 
trates such  a  reaction.  A  floating  Amoeba  will  thus  spread  out  on  the 
substratum,  on  the  surface  film,  or,  so  far  as  possible,  on  small  masses 
of  debris  suspended  in  the  water. 

An  Amoeba  which  is  moving  along  a  surface  also  shows  at  times  a 
positive  reaction  to  mechanical  stimuli  by  turning  toward  small  objects 
with  which  it  comes  in  contact  at  one  side  of  the  anterior  end.  This  reac- 
tion takes  place  very  frequently  in  the  normal  locomotion  of  Amoeba, 
but  I  have  not  been  able  to  produce  it  experimentally  by  touching  one 
side  of  the  animal  with  a  glass  rod.  This  is  because  it  is  difficult  to 
give  a  touch  so  light  that  it  shall  not  induce  the  negative  reaction.  I 
shall  give  a  detailed  account  of  reactions  that  probably  belong  here  in 
connection  with  the  account  of  food  reactions  (pp.  196-202,  and  Figs. 


d  c 

Fig.  65.* 

73-76).     As  will  there  be  shown,  the  reaction  is  often  long  continued 
and  rather  complicated. 

Le  Dantec  (1895)  gave  a  good  account  of  the  positive  reaction  of 
Amoeba,  as  shown  in  its  spreading  out  on  solids. 

NEGATIVE   REACTION. 

I  have  studied  the  negative  reaction  to  mechanical  stimuli  by  touch- 
ing a  spot  on  one  side  or  end  of  the  animal  with  the  tip  of  a  fine  glass 
rod.  A  glass  rod  may  easily  be  so  drawn  out  that  its  tip  is  as  fine  as 
the  tip  of  a  pseudopodium,  and  with  some  practice  it  is  possible  to  give, 
under  the  microscope,  in  the  open  drop,  very  precisely  localized  stim- 
uli with  this. 

We  will  first  examine  the  reaction  to  a  rather  strong  stimulus  at  the 
anterior  edge  of  an  Amoeba  that  is  creeping  forward  with  outspread 
anterior  end  and  contracted  posterior  end  in  the  usual  way.  The  tip 
of  the  glass  rod  is  thrust  sharply  against  the  anterior  edge,  producing 

*  Fig.  65. — Positive  reaction  to  a  mechanical  stimulus  in  Amoeba,  in  side  view. 
A  floating  Amoeba  comes  in  contact  by  one  of  its  pseudopodia  with  a  solid  (a); 
it  thereupon  passes  to  the  solid,  withdrawing  the  other  pseudopodia  {b  and  c). 
See  text. 


THE    MOVEMENTS   AND    REACTIONS    OF   AMCEBA.  183 

a  depression  in  the  ectosarc  that  may  last  for  some  time  (Fig.  66), 
(We  will  suppose  that  the  thrust  does  not  detach  the  Amoeba  from  the 
surface,  as  sometimes  happens.)  At  once  the  anterior  portion  of  the 
Amoeba  ceases  to  advance.  It  remains  quiet  for  a  definite  interval, 
which  I  should  judge  to  be  about  a  second,  while  the  current  from  behind 
continues  to  move  forward.  As  a  result  of  the  stoppage  at  the  anterior 
edge  there  is  a  heaping  up  of  the  protoplasm  in  the  middle  of  the  body. 
After  about  a  second  the  part  stimulated  begins  to  contract  and  currents 
start  backward  from  it.  Thus  the  currents  from  the  two  ends  meet  in 
the  middle,  often  producing  a  further  heaping  up  in  this  region.  Usu- 
ally, however,  the  ectosarc  of  one  side  of  the  Amoeba  quickly  gives 
way  and  a  new  pseudopodium  starts  out  laterally.  As  a  rule  this  new 
pseudopodium  is  formed  near  the  original  anterior  margin,  often  at  the 
very  edge  of  the  area  directly  affected  by  the  stimulus  (Fig.  66).  The 
reason  for  this  is  evident.  Only  this  anterior  half  of  the  Amoeba  is 
expanded  and  attached  to  the  substratum,  the  posterior  half  being  free 
and  contracted.  It  is,  therefore,  much  easier  to  continue  locomotion 
by  sending  out  pseudopodia  somewhere  in  the  attached  region  than 
behind  it.  If  sent  out  in  the  unattached  region,  the  original  contraction 
would  have  to  be  overcome,  and  no  locomotion  could  occur  until  the 
pseudopodium  had  (by  chance  ?)  come  in  contact  with  the  substratum 
and  become  attached  to  it.  By  sending  out  pseudopodia  thus  in  some 
portion  of  the  attached  region,  the  movement  is,  in  a  certain  sense,  a 
continuation  of  that  which  was  taking  place  before  stimulation,  though 
in  a  different  direction.  The  Amoeba  follows  a  path  which  forms  an 
angle  with  its  previous  one. 

The  course  of  the  reaction  may  vary  considerably  from  that  above 
described.  If  the  stimulus  is  weak  the  reaction  may  consist  merely  in 
a  stoppage  at  the  point  stimulated  without  any  contraction  there.  The 
current  from  behind  continues  ;  a  pseudopodium  breaks  out  at  one  side 
of  the  region  stimulated,  and  the  Amoeba  moves  in  the  direction  so 
indicated.  If  the  stimulus  is  very  weak  the  current  may  cease  only 
for  an  instant  in  the  region  stimulated,  then  continue  as  before ;  the 
direction  of  progress  thus  remains  unchanged. 

If  the  stimulus  is  very  strong  the  contraction  which  takes  place  at 
the  region  stimulated  may  be  very  marked,  resulting  in  the  formation 
of  strong  folds  in  this  region.  The  contraction  may  include  the  entire 
anterior  end  of  the  Amoeba.  Such  a  contraction  destroys  the  attach- 
ment to  the  substratum,  and  the  new  pseudopodium  now  bursts  out  in 
some  part  of  what  was  the  posterior  end  of  the  body.  The  new  course 
followed  may  then  be  at  right  angles  to  the  old  one,  or  at  any  greater 
angle,  or  the  course  may  be  exactly  reversed,  the  new  pseudopodium 
being  formed  at  the  posterior  end.     If  the  posterior  end  was  much 


.84 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


wrinkled  or  bore  a  pronounced  roughened  "  tail,"  it  is  to  be  noticed 
that  the  new  pseudopodium  does  not  flow  out  directly  from  this,  but  to 
one  side  of  it  or  above  it  (Fig.  6"]).  Then  as  the  Amceba  moves  in  the 
reverse  direction  the  body  passes  the  old  "  tail,"  which  finally  brings 
up  the  rear  again,  fusing  with  the  rough  area  produced  by  contraction  of 
the  region  stimulated  (Fig.  67,  b).  Of  course,  the  new  pseudopodium 
formed  must  come  in  contact  with  the  substratum  and  become  attached 
to  it  before  locomotion  in  the  new  direction  can  occur.  Sometimes 
the  new  pseudopodium  formed  is  sent  directly  upward  into  the  water ; 
then  there  is  no  locomotion  until  the  Amoeba  topples  over,  bringing 
the  new  pseudopodium  in  contact  with  the  substratum. 

At  times  when  the  anterior  end  is  stimulated,  two  new  pseudopodia 
are  sent  out  in  opposite  directions  on  each  side  of  the  region  stimulated. 


Fig.  66.* 


Fig.  67.1 


Both  evidently  pull  on  the  Amoeba,  which  becomes  drawn  out  to  form 
a  narrow  isthmus  between  them.    Finally  one  end  pulls  the  other  away 
from  its  attachment  to  the  bottom  ;  the  latter  then  contracts,  and  loco- 
motion continues  in  the  direction  of  the  prevailing  pseudopodium. 
There  is  at   times  a  peculiar  additional   feature  of  the  reaction  to 


♦  Fig.  66. — Negative  reaction  to  a  mechanical  stimulus  in  Amoeba.  An  Amoeba 
advancing  in  the  direction  shown  by  the  arrows  is  stimulated  strongly  with  the 
glass  rod  at  the  anterior  end  (at  a).  Thereupon  the  currents  are  changed  and  a 
new  pseudopodium  sent  out  as  at  b. 

tFiG.  67. — Negative  reaction  to  a  mechanical  stimulus  when  the  anterior  end 
is  strongly  stimulated.  The  arrow,  a;,  shows  the  original  direction  of  motion ; 
the  arrows  in  a  show  the  currents  immediately  after  the  stimulation.  A  large 
pseudopodium  is  sent  out  from  above  and  to  one  side  of  the  former  tail  (/),  as  is 
shown  by  the  broken  outline.  In  b  this  pseudopodium  has  come  in  contact  with 
the  bottom ;  the  arrows  show  the  direction  of  the  currents  and  of  locomotion  at 
this  time;  t,  the  original  tail;  /',  the  new  tail  formed  by  the  contraction  of  the 
anterior  end. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  1 85 

Strong  stimuli.  In  some  cases  there  is  for  an  instant  after  a  strong 
stimulation  at  the  anterior  end  a  sudden  rush  of  protoplasm  toward 
the  region  stimulated  ;  this  is  immediately  followed  by  the  stoppage 
and  contraction  above  described.  Apparently  this  sudden  rush  toward 
the  point  stimulated  is  produced  as  follows :  The  first  effect  of  the 
additional  contraction  caused  by  the  stimulus  is  to  release  a  certain 
amount  of  surface  at  the  posterior  edge  of  the  attached  area  from  its 
attachment  to  the  substratum.  This  portion  was  nearly  ready  to  become 
released  in  the  ordinary  course  of  events,  so  that  probably  a  very  slight 
shock  would  release  it  at  once.  Now,  as  I  have  shown  on  p.  167,  when 
a  portion  of  the  lower  surface  of  the  Amoeba  is  suddenly  released  from 
the  substratum,  it  contracts,  causing  a  strong  forward  current.  This 
is  what  happens  in  the  case  under  consideration.  Later  this  current  is 
stopped  by  the  effect  of  the  stimulus  in  the  anterior  region. 

The  surface  currents  in  the  reaction  are  changed  in  the  same  way  as 
are  the  internal  currents,  and  are  throughout  congruent  with  them. 
Particles  moving  forward  on  the  upper  surface  of  the  Amoeba  stop 
after  the  stimulus,  then  move  in  the  direction  of  the  new  forward 
current.  This  has  been  illustrated  in  detail  for  Amoeba  verrucosa 
(p.  143),  so  that  we  need  not  go  into  the  matter  further  here. 

The  essential  features  of  the  negative  reaction  to  a  mechanical  stim- 
ulus are,  then,  a  contraction  of  the  region  stimulated,  with  the  formation 
of  a  new  pseudopodium  in  what  may  be  considered  the  region  of  least 
resistance,  followed  by  a  change  in  the  direction  of  the  currents  of 
protoplasm,  thus  altering  the  course  of  the  Amoeba. 

By  repeated  mechanical  stimuli  it  is  possible  to  drive  the  Amoeba  in 
any  desired  direction.  I  have  at  times  made  use  of  this  possibility  in 
order  to  bring  into  contact  two  Amoebae  or  two  pieces  of  an  Amoeba 
whose  courses  lay  in  different  directions.  Such  driving  of  an  Amoeba 
requires  considerable  skill  and  a  rather  high  tension  on  the  part  of  the 
operator.  The  new  pseudopodium  formed  is  stimulated  to  withdraw 
as  often  as  it  is  formed,  until  it  finally  starts  out  in  the  desired  direction. 
If  it  were  possible  to  stimulate  all  of  one  side  of  an  Amoeba  at  once  it 
would,  of  course,  be  driven  directly  toward  the  opposite  side,  even 
though  the  stimulus  were  weak.  With  chemical  and  some  other  stimuli, 
as  we  shall  see,  this  is  possible.  With  mechanical  stimuli  it  is  usually 
possible  only  when  the  stimulus  is  very  strong.  By  drawing  the  tip 
of  the  glass  rod  along  one  side  of  a  moving  Amoeba,  it  is  often  possible 
to  make  it  flow  directly  toward  the  opposite  side,  as  illustrated  in  Fig. 
6^,  This  point  is  important  for  an  understanding  of  the  effects  of  such 
stimuli  as  chemicals,  heat,  and  light. 

When  a  single  pseudopodium  is  stimulated,  it  is  merely  withdrawn, 
wrinkling  and  becoming  warty  in  the  usual  way ;  there  may  be  no 
other  effect  on  the  movement  of  the  animal. 


i86 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


Among  the  sweeping  statements  that  one  finds  current  in  regard  to 
the  behavior  of  these  low  organisms  is  one  to  the  effect  that  the  Protist 
does  not  avoid  an  obstacle  in  its  path.  This  statement  is  made  for 
example  by  Ziehen,  in  his  excellent  Leitfaden  der  fhysiologischen 
Psychologic*  It  is  worth  while,  therefore,  to  describe  in  connection 
with  the  reactions  to  mechanical  stimuli  just  how  Amoeba  avoids  an 
obstacle.  Let  us  take  a  concrete  case.  An  AmcEba  creeping  with  a 
broad,  flat  anterior  end  came  in  contact  at  the  middle  of  its  anterior 
edge  with  the  end  of  a  long  filament  of  some  sort  (Fig.  69).  The 
particular  spot  touched  (c)  ceased  to  move  forward,  becoming  entirely 
quiet  (reaction  to  a  weak  mechanical  stimulus).  On  each  side  of  it 
motion  continued  as  before,  so  that  after  a  time  the  filament  projected 
into  a  notch  in  the  middle  of  the  anterior  edge.     Then  gradually  the 


Fig.  694 

forward  movement  ceased  on  the  side  x  and  increased  at  j,  the  pseudo- 
podium  X  contracted,  and  its  endosarc  passed  into  jk-  The  animal  then 
continued  its  course  in  the  direction  indicated  by  y.  It  had  thus 
changed  its  path  so  as  to  avoid  the  obstacle  presented  by  the  filament. 
Such  cases  are  often  seen. 


♦  "  Hindernissen  weichen  dieselben  nicht  aus  "  (/.  c,  p.  11). 

tFiG.  68. — An  Amceba  moving  in  the  direction  shown  by  the  arrows  in  the 
unbroken  outline  is  stimulated  by  drawing  the  tip  of  a  glass  rod  along  one  side, 
from  a  to  b.  Thereupon  a  pseudopodium  bursts  out  of  the  opposite  side,  as 
shown  by  the  broken  outline,  and  the  Amoeba  continues  locomotion  in  the  direc- 
tion so  indicated. 

\  Fig.  69. — Method  by  which  Amoeba  avoids  an  obstacle.  The  Amoeba  a-b-c-d 
comes  in  contact  at  c  with  the  end  of  a  filament.  Thereupon  motion  at  c  ceases, 
■while  elsewhere  it  continues,  so  that  after  a  time  the  Amoeba  has  the  position 
shown  by  the  broken  outline.  Then  the  currents  become  changed  in  x;  its  sub- 
stance passes  into  the  pseudopodium  jk>  and  the  AmcBba  continues  to  move  in  the 
direction  indicated  by  the  arrows  in  the  lower  figure. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  187 

Much  more  striking  cases  of  the  regulation  of  the  movement  in 
accordance  with  the  position  and  changes  in  position  of  outward  things 
C  automatic  acts/'  Ziehen,  /.  c.)  than  are  found  in  such  a  reaction,  or 
even  than  in  the  possibility  of  driving  an  Amoeba,  will  be  described 
in  the  account  of  the  food  reactions  (p.  196). 

REACTIONS   TO   CHEMICAL   STIMULI. 

By  analogy  with  the  effects  of  mechanical  stimuli  we  might  expect 
to  find  a  positive  reaction  to  chemical  stimuli.  Such  reactions  doubt- 
less occur,  but  I  have  not  been  able  to  demonstrate  them  under  experi- 
mental conditions,  and,  so  far  as  I  am  aware,  no  one  else  has  succeeded 
in  doing  this.  Stahl  (18S4)  has  shown  the  corresponding  reaction  to 
take  place  in  the  myxomycete  plasmodium.  Verworn  (1S90,  p.  456) 
records  an  observation  which  he  refers  with  much  probability  to  a 
positive  reaction  to  a  chemical  stimulus  in  Difflugia.  If  two  conjuga- 
ting Difflugias  were  separated,  they  crept  directly  together  again,  and 
it  is  difficult  to  see  how  the  movements  could  have  been  directed  save 
by  some  chemical.  But  I  believe  there  is  no  instance  of  positive  chemo- 
taxis  in  Rhizopoda  where  the  nature  of  the  active  substance  is  known 
and  the  reaction  was  controlled  experimentally.  A  number  of  striking 
positive  reactions,  which  should  probably  be  attributed  partly  to  chemi- 
cal stimuli,  are  described  later  in  connection  with  the  attempts  of 
Amoeba  to  obtain  food  (p.  196). 

The  same  state  of  affairs  has  existed  hitherto  with  regard  to  our 
knowledge  of  a  negative  reaction  to  chemicals.  In  Amoeba  it  is,  how- 
ever, not  difficult  to  produce  such  reactions  experimentally. 

For  this  purpose  only  a  small  amount  of  the  chemical  must  be  used, 
so  that  it  can  act  on  but  a  limited  portion  of  the  body  of  the  animal. 
If  there  is  a  considerable  amount  of  the  solution,  diffusing  over  a  large 
area,  it  reaches  a  strength  sufficient  to  cause  a  reaction  at  about  the  same 
time  over  the  whole  body  of  the  Amoeba  ;  thus  the  reaction  is  a  general 
one,  not  involving  movement  in  a  definite  direction.  To  produce  a 
directed  reaction  there  must  be  a  decided  difference  in  the  strength  of 
the  solution  on  two  sides  of  the  organism. 

The  easiest  method  of  producing  the  reaction,  and  the  one  giving  at 
the  same  time  the  most  striking  results,  is  to  dip  the  moistened  tip  of 
a  capillary  glass  rod  into  powdered  methyl  green  or  methyline  blue ; 
then  to  bring  this  near  one  side  or  end  of  the  Amoeba,  in  an  open  drop 
of  water.  The  chemical  diffuses  in  a  colored  cloud  ;  the  reaction  takes 
place  when  the  edge  of  this  cloud  comes  in  contact  with  the  Amoeba. 

The  reaction  is  essentially  the  same  as  that  to  mechanical  stimuli. 
The  region  stimulated  stops  suddenly,  and  about  a  second  later  con- 
tracts, while  a  current  moves  away  from  the  side  stimulated.  This 
may  meet  the  previously  existing  current  coming  from  the  original 


^^■■^-■■- i 


l88  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

posterior  end  ;  the  two  turn  to  one  side,  and  a  pseudopodium  starts  out 

in  a  new  place.     If  the  stimulation  took  place  at  the  anterior  end  and 

was  limited  to  a  small  area,  the  new  pseudopodium  starts  out  at  one 

side  of  the  original  anterior  end  ;  the  new  course  followed,  therefore, 

forms  only  a  slight  angle  with  the  former  one  (Fig.  71,  a).     But  if  the 

stimulus  affects  all  of  one  side  of  the  body,  or  a  still  greater  portion  of 

its  area,  pseudopodia  are  sent  out  on  the  opposite  side ;  the  Amceba 

then  creeps  directly  away  from  the  source  of  diffusion  of  the  chemical. 

This  gives  a  typical  case  of  negative  "  chemotaxis,'*  the  longitudinal 

axis  being  in  the  line  of  diffusion  of  the  ions  or  molecules,  with  the 

anterior  end  directed  away  from  the  source  of  diffusion  (Fig.  70) .     It 

will  be  noted  that  the  reaction  is  exactly  the  same  as  that  produced  by 

mechanical  stimuli ;  in  "  chemotaxis,"  where  the  animal  is  *'  oriented," 

we  have  the  same  process  as  in  ''  driving"  the  Amoeba  in  a  definite 

direction  by  means  of  mechanical  stimuli.     All  movement  toward  the 

chemical  is  inhibited,  because  this  brings  the  protoplasm  into  a  region 

-^•''**'*>''^X'-  where  it  is  stimulated.     Pseudopodia  can  be  sent  out, 

,^^^^^j^^._    therefore,  only  on  the  side  away  from  the  chemical, 

:;^^   and  movement  can  occur  only  in  that  direction. 

The  surface  currents  are  changed  exactly  as  are  the 

internal   currents ;    the   facts  here   are  identical  with 

those  described  for  mechanical  stimuli  (p.  185).    The 

„  ^  surface  currents  are  thus  awav  from  a  chemical  which 

Fig.  70.*  /  "     T^ 

causes  a  negative  reaction  (see  Fig.  42,  p.  144). 

A  number  of  variations  in  the  reactions  to  chemicals  are  shown  in 
Fig.  71,  all  of  them  taken  from  actual  experiments.  As  the  figure 
shows,  after  stimulation  frequently  two  pseudopodia  start  out  in  oppo- 
site directions,  one  finally  prevailing  over  the  other  (Fig.  71,  d). 

The  contraction  due  to  the  chemical  is  often  very  marked,  the  ecto- 
sarc  against  which  the  chemical  impinges  shrinking  sharply  together 
and  becoming  covered  with  folds  (Fig.  71,  6).  With  methyl  green  as 
the  stimulus,  the  surface  touched  by  the  chemical  is  sometimes  stained, 
so  that  the  shrinkage  in  area  is  very  precisely  definable.  With  a  solu- 
tion of  NaCl  the  shrinkage  is  extreme,  while  the  opposite  side  spreads 
out  widely,  compensating,  or  more  than  compensating,  for  the  decrease 
in  surface  caused  by  the  shrinkage  (Fig.  71,  d). 

The  effect  of  substances  not  in  the  form  of  powder  was  tried  in  the 
following  manner :  A  glass  tube  was  drawn  out  to  a  very  fine  point, 
and  into  it  was  introduced  some  of  the  solution  to  be  tested.  The  fine 
point  of  the  tube  was  then  brought  close  to  the  Amoeba.     Some  of  the 


*  Fig.  70. — Diagram  of  *'  negative  chemotaxis  "  in  Amoeba.  A  chemical  diffuses 
from  a  center,  as  indicated  b_y  the  radii ;  the  Amoeba  reacts  in  such  a  way  as  to 
creep  directly  away  from  the  sourceofdifFusion,ina  line  with  the  radii  of  diffusion. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


189 


chemical  flowed  slowly  out,  and  its  action  on  the  Amoeba  could  be 
observed.  The  results  obtained  by  this  method  were  very  clear.  A 
negative  reaction,  as  described  above,  was  observed  in  this  way  for 
solutions  of  the  following  substances :  Methyl  green,  methyline  blue, 
sodium  chloride,  potassium  nitrate,  potassium  hydroxide,  sodium  car- 
bonate, acetic  acid,  hydrochloric  acid,  cane  sugar.  Of  these  substances 
relatively  strong  solutions  were  used  (usually  about  i  per  cent).  Of 
course,  the  solution  which  came  in  contact  with  the  Amceba  was  much 
weaker  than  this,  being  diluted  by  the  surrounding  water.  Emphasis 
was  not  laid  on  the  quantitative  aspect  of  the  matter ;  the  question  pro- 
posed was,  How  does  the  animal  react .'^  and  not.  How  much  is  required 
to  produce  the  reaction  ?     Therefore,  different  strengths  were  employed 


Fig.  71.* 

till  one  was  found  that  was  eff^ective.  In  any  case,  I  do  not  know  of 
any  way  in  which  one  could  determine  the  exact  strength  of  the  solution 
which  comes  in  contact  with  the  surface  of  the  Amoeba. 


♦Fig.  71. — Variations  in  reactions  of  Amceba  to  chemicals.  The  dotted  area 
represents  in  each  case  the  diifusing  chemical.  The  arrows  show  the  direction 
of  the  protoplasmic  currents. 

a.  The  chemical  (methyl  green)  diffuses  against  the  anterior  end  of  an  advanc- 
ing Amoeba;  the  latter  reacts  by  sending  out  a  new  pseudopodium  at  one  side  of 
the  anterior  end  and  moving  in  the  direction  so  indicated. 

b.  A  solution  of  NaCl  diffuses  against  the  right  side  of  a  moving  Amoeba  (i). 
The  side  affected  contracts  and  wrinkles  strongly,  while  the  opposite  side  expands 
(2),  the  currents  flowing  in  the  direction  indicated  by  the  arrows. 

c.  A  solution  of  NaCl  diffuses  against  the  anterior  end  of  an  advancing  Amceba. 
The  course  is  thereupon  reversed,  a  broad  pseudopodium,  shown  by  the  dotted 
line,  pushing  out  from  the  upper  surface  of  the  posterior  end  above  the  tail. 

d.  Asolution  of  methyline  blue  diffuses  against  the  anteriorendof  an  advancing 
Amoeba  (i);  thereupon  a  pseudopodium  is  sent  out  on  each  side  of  the  posterior 
end  at  right  angles  with  the  original  course  (2).  Into  these  pseudopodia  are 
drawn  the  body  and  the  tail  (3). 


igO  THE   BEHAVIOR    OF   LOWER    ORGANISMS. 

As  a  control  experiment,  distilled  water  was  used  in  the  tube  in 
place  of  a  chemical  in  solution.  Amoeba  was  found  to  react  negatively 
to  this  also,  though  the  reaction  was  less  marked  than  with  most  of  the 
chemicals.  But  this  result,  of  course,  rendered  the  experiments  with 
solutions  of  chemicals  in  the  tube  indecisive,  as  the  Amoeba  may  have 
reacted  to  the  distilled  water  in  which  the  solutions  were  made  up. 
The  solutions  were,  therefore,  made  up  with  culture  water,  and  the 
same  results  were  obtained  as  before. 

The  results  with  the  chemicals  show  merely  that  Amoeba  responds 
negatively  to  almost  any  solution  differing  markedly  from  that  in  which 
the  animal  is  immersed,  the  precise  chemical  composition  of  the  solu- 
tion being  of  little  consequence.  The  animal  responded  negatively  not 
only  to  distilled  water  and  to  the  chemicals  mentioned,  but  also  to  tap 
water,  and  to  water  taken  from  other  cultures  than  that  in  which  the 
specimens  occurred. 

REACTIONS   TO    HEAT. 

Verworn  (1889,  pp.  64-67)  studied  the  directive  influence  of  heat  on 
the  locomotion  of  Amoeba  by  concentrating  the  sunlight  on  a  small  por- 
tion of  the  slide  and  leaving  the  rest  dark,  then  observing  the  behavior 
of  the  Amoeba  on  coming  to  the  boundary  of  this  lighted  and  heated  area. 
The  effects  of  the  light  proper  were  excluded  by  control  experiments. 
It  was  found  that  on  coming  to  the  heated  area  Amoeba  remained  quiet 
a  moment,  then  contracted  on  the  heated  side,  and  sent  out  a  pseudopo- 
dium  on  the  opposite  side.  It  then  crept  away  in  the  direction  indicated 
by  this  pseudopodium  ("  negative  thermotropism"). 

My  experiments  differed  from  those  of  Verworn  in  employing  con- 
ducted heat  in  place  of  radiant  heat ;  thus  there  was  no  possibility  of 
a  complication  from  the  effects  of  light.  As  Verworn  sets  forth,  it  is 
difficult  to  warm  only  one  side  of  so  small  an  object  as  an  Amoeba.  I 
succeeded,  however,  in  doing  this  in  a  very  simple  manner.  For  each 
experiment  an  Amoeba  was  selected  that  was  creeping  on  the  under 
surface  of  the  cover  glass.  This  was  placed  in  focus  under  an  objective 
of  a  considerable  focal  distance,  yet  of  high  enough  power  so  that  the 
internal  movements  could  be  seen.  A  needle  was  then  heated  in  a  flame 
and  its  point  was  brought  against  the  cover  glass  a  short  distance  in 
advance  of  the  Amoeba.  Control  experiments  had  shown  that  the  use 
of  a  needle  at  room  temperature  had  no  effect. 

If  the  heated  needle  was  placed  at  a  proper  distance  from  the  Amoeba, 
the  phenomena  follow  as  described  by  Verworn  (/.  c).  There  was  a 
short  pause,  then  the  side  next  to  the  needle  contracted.  A  current 
of  protoplasm  passed  toward  the  opposite  side,  at  times  meeting  the 
current  already  in  existence.  A  new  pseudopodium  was  sent  out,  either 
on  the  side  opposite  the  needle,  or,  in  many  cases,  in  a  direction  inter- 


THE    MOVEMENTS    AND   REACTIONS   OF   AMCEBA.  I9I 

mediate  between  this  and  the  original  one.  The  phenomena  are  in  all 
respects  identical  with  those  seen  in  the  negative  reaction  to  mechanical 
stimuli.  If  the  needle  is  brought  a  little  nearer,  so  that  the  heat  acts 
more  strongly,  there  is  a  sudden  strong  contraction  of  the  side  affected. 

Simultaneously  with  this  there  is  often,  as  in  the  case  of  strong 
mechanical  stimuli,  a  sudden  rush  of  the  internal  fluid  toward  the  side 
stimulated.  This  lasts  but  an  instant  and  is  succeeded  by  a  current 
away  from  the  stimulated  side,  the  formation  of  a  pseudopodium  on  the 
unstimulated  side,  and  locomotion  in  that  direction.  The  sudden  rush 
of  internal  contents  toward  the  side  affected  is,  I  think,  clearly  due  to 
the  cause  suggested  under  mechanical  stimuli.  Part  of  the  posterior 
portion  of  the  attached  area  of  the  Amceba  is  loosened  from  the  substra- 
tum by  the  sudden  contraction  at  the  front  end  ;  this  portion,  therefore, 
contracts  quickly  and  sends  a  current  forward,  as  described  on  p.  168. 

When  the  heat  is  still  more  powerful  the  entire  Amoeba  is  affected. 
It  contracts  and  at  the  same  time  loses  its  attachment  to  the  substratum. 
There  is  a  strong  momentary  rush  of  the  internal  fluid  toward  the  end 
which  had  been  anterior,  due  to  the  cause  set  forth  in  the  preceding 
paragraph.  This  ceases  and  the  body  becomes  very  irregular  and  ceases 
to  move. 

The  reaction  to  local  stimulation  by  heat  is  thus  of  essentially  the 
same  character  as  the  reaction  to  mechanical  stimuli  and  to  chemicals. 

Like  Verworn  (1889,  p.  67),  I  have  been  unable  to  obtain  a  reaction 
to  cold  in  Amoeba. 

REACTIONS    TO    OTHER    SIMPLE    STIMULI. 

The  reactions  of  Amoeba  to  electricity  and  to  light  have  been  thor- 
oughly studied  by  other  authors,  so  that  it  will  not  be  necessary  to  treat 
them  in  detail  here.  Only  certain  especially  important  points  will  be 
touched  upon. 

The  reactions  of  Amoeba  to  the  continuous  electric  current  have 
been  studied  in  detail  by  Verworn  (1890,  a;  1897).  I  have  repeated  the 
experiments  in  order  to  determine  by  observation  the  direction  of  the 
surface  currents  of  protoplasm  during  the  reaction.  For  this  purpose 
soot  was  mingled  with  the  water  containing  the  Amoebae,  and  the  elec- 
tric current  was  passed  through  the  preparation.  The  typical  reac- 
tion as  described  by  Verworn  was  observed  in  many  cases,  but  the 
surface  currents,  of  course,  cannot  be  seen  unless  soot  is  resting  upon  or 
is  attached  to  the  surface  of  the  animal,  which  happens  only  rarely. 
Finally  a  specimen  of  Amoeba  froteus  was  observed  with  a  string  of 
soot  particles  attached  to  one  side  (Fig.  72).  The  electric  current  was 
then  passed  through  the  preparation  in  such  a  way  that  the  side  bearing 
the  soot  was  next  to  the  anode  (Fig.  72,  a).     The  Amoeba  thereupon 


192 


THE    BEHAVIOR    OF    LOWER    ORGANISMS, 


turned  and  began  to  move  toward  the  cathode  (<$) ,  dragging  the  parti- 
cles of  soot  behind  it  for  a  short  distance.  Then  the  string  of  soot  began 
to  pass  forward  on  the  upper  surface,  in  the  usual  way  (c,  d).  This 
continued  until  the  soot  reached  the  anterior  edge  and  dropped  off  the 
surface  of  the  Amoeba  {e).  The  currents  on  the  upper  surface  of  Amoeba 
are,  then,  forward  (toward  the  cathode)  in  the  reaction  to  the  electric 
current,  as  well  as  in  other  cases. 

On  reversing  the  current  the  specimen  described  above  began  to 
move  in  the  opposite  direction  toward  the  new  cathode.  In  this  and 
many  other  observed  cases  of  the  reversal  of  movement  under  the  in- 
fluence of  the  electric  current,  the  reversal  occurred  in  the  same  manner 
as  when  induced  by  other  stimuli  (see  p.  183).  That  is,  the  new  pseudo- 
podium  was  sent  out  from  one  side  of  the  attached  (anterior)  half  of  the 
body,  changing  the  course  a  certain  amount.  From  this  new  portion 
another  new  pseudopodium  was  sent  out  on  the  side  toward  the  anode, 


Fig.  72.* 

and  this  continued  until  the  direction  of  movement  had  been,  by  a 
gradual  process,  completely  reversed.  Verworn  (/.  c.)  describes  cases 
in  which  the  reversal  takes  place  suddenly,  the  new  pseudopodium 
appearing  at  the  original  posterior  end.  This  happens  also  at  times,  as 
we  have  seen,  in  the  reactions  to  other  stimuli  (p.  183).  It  is  to  be  noted 
that  the  reaction  to  the  electric  current  is  exactly  that  which  would 
occur  if  the  animal  were  strongly  stimulated  on  the  anode  side. 

Verworn  (1889),  Davenport  (1897),  and  Harrington  &  Leaming 
(1900)  have  studied  the  reaction  of  Amoeba  to  light.  Verworn  (/.  c.^ 
p.  97)  found  that  light  falling  perpendicularly  on  one-half  of  the  Amoeba 
produced  no  reaction.  Davenport  (/.  c,  pp.  186,  188)  confirmed  this 
result,  but  showed  that  when  the  light  falls  obliquely  from  one  side  on 
Amoeba  the  animal  reacts  negatively.  Harrington  &  Leaming  (/.  c.) 
found  that  when  white  light  falls  upon  the  Amoeba  from  above  the 


♦Fig.  72. — Movement  of  particles  attached  to  the  outer  surface  of  Amceba  in 
the  reaction  to  the  electric  current.  Anode  and  cathode  are  represented  by  the 
plus  C-}-)  and  minus  ( — )  signs,  a,  Form  and  direction  of  movement  of  the  Amoeba 
before  the  current  is  made  ;  at,  a  chain  of  soot  particles  attached  to  one  side  ;  b,  c, 
d,  e,  successive  stages  during  the  reaction.  The  chain  of  soot  particles  {x)  passes 
to  the  upper  surface  and  forward,  reaching  at  e  the  anterior  edge. 


J 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I93 

movements  cease,  while  in  red  light  they  begin  again ;  lights  of  other 
colors  have  various  intermediate  effects. 

It  seems  to  the  writer  that  further  experimentation  is  desirable  on  the 
results  of  a  perpendicular  illumination  of  one-half  the  animal.  The 
difference  between  the  results  thus  far  obtained  from  such  illumination 
and  those  from  Davenport's  experiments  where  light  is  admitted  from 
one  side  is  very  remarkable.  If  this  difference  is  constant,  it  is  of  much 
significance  for  the  theory  of  light  reactions.  Possibly  the  lack  of  re- 
action when  but  one-half  the  animal  is  illuminated  may  be  accounted 
for  as  follows  :  When  one  end  of  an  Amoeba  is  illuminated  from  below, 
as  in  Verworn's  experiments,  it  is  difficult  or  impossible  to  keep  this 
difference  of  illumination  constant  for  any  considerable  period.  If  the 
Amoeba  does  not  react  at  once  it  passes  completely  into  the  lighted  area, 
where  there  is  no  cause  for  changing  the  direction  of  movement.  On 
the  other  hand,  in  the  case  of  light  falling  obliquely  from  one  side,  the 
different  action  of  the  light  on  the  two  sides  is  constant,  so  that  in  time 
a  reaction  is  produced.  The  slowness  of  Amoeba  in  reacting  is  such 
as  to  make  this  possibility  worth  considering.  For  further  work  from 
this  point  of  view  a  source  of  powerful  artificial  light  is  needed.  This 
I  have  not  had  at  command  during  the  present  investigation. 

It  is  evident  that  the  reaction  of  Amoeba  to  light  falling  from  one  side 
is  exactly  that  which  would  be  produced  were  the  Amoeba  strongly 
stimulated  on  the  side  on  which  the  light  impinges. 

For  an  account  of  the  reactions  of  Amoeba  to  general  (not  localized) 
stimuli,  see  Verworn,  1888,  and  the  Allgemeine  Physiologie  of  the 
same  author. 

SOME  COMPLEX  ACTIVITIES. 

Under  this  heading  I  propose  to  describe  certain  striking  phenomena 
in  the  behavior  of  Amoeba,  the  stimuli  to  which  are  complex  or  not 
sharply  definable.  These  concern  the  reactions  of  Amoeba  to  food  and 
to  injuries,  and  the  relations  of  one  Amoeba  to  another. 

ACTIVITIES    CONNECTED   WITH   FOOD-TAKING. 

The  behavior  of  Amoeba  in  taking  food  or  in  attempting  to  take  food 
shows  many  features  of  great  interest  for  one  attempting  to  understand 
the  behavior  of  these  organisms.  I  have  observed  the  process  of  food- 
taking  many  times,  and  will  describe  it,  together  with  a  number  of 
related  activities. 

Let  us  take  a  concrete  case.  A  specimen  oi  Amoeba proteus  was  creep- 
ing about  on  a  slide  which  contained  many  spherical  cysts  of  Euglena 
viridis.  One  of  these,  which  was  not  attached  to  the  bottom  (as  most 
of  them  are),  was  lying  in  the  path  of  the  Amoeba.  The  latter  in  its 
forward  movement  came  against  the  cyst  and  pushed  it  forward  a  short 
distance.     There  was  no  evidence  of  a  tendency  of  the  cyst  to  adhere  to 


194  '^"^  BEHAVIOR  OF  LOWER  ORGANISMS. 

the  Amoeba  ;  on  the  contrary,  it  was  pushed  ahead  as  fast  as  the  Amoeba 
moved.  The  Amoeba  now  put  out  a  pseudopodium  on  each  side  of  the 
cyst,  while  that  part  of  the  protoplasm  immediately  behind  it  stopped 
moving.  Thus  the  cyst  was  enclosed  in  a  little  bay.  On  bringing  the 
upper  surface  of  the  cyst  into  focus  it  could  be  seen  that  a  thin  layer  of 
protoplasm  was  also  sent  over  the  cyst.  The  two  pseudopodia  enclosing 
the  cyst  now  bent  over  at  their  free  ends,  so  that  the  cyst  could  not  be 
pushed  away  by  movement  of  the  Amoeba.  The  two  free  ends  finally 
met,  leaving  only  a  sort  of  transparent  seam  to  show  the  place  of  con- 
tact. Later  this  disappeared,  and  the  two  pseudopodia  fused  completely. 
At  the  end  of  two  minutes  from  the  time  that  the  Amoeba  first  came  in 
contact  with  it  the  cyst  was  completely  enclosed.  The  Amoeba  now 
remained  perfectly  quiet  for  one  minute,  then  crept  away,  carrying  the 
cyst  with  it.  With  the  cyst  had  been  taken  in  some  water,  so  that  it 
was  enclosed  in  a  vacuole  a  little  larger  than  itself.  The  walls  of  the 
vacuole  had  exactly  the  appearance  of  the  ectosarc  on  the  outer  surface 
of  the  Amoeba. 

This  is  essentially  the  method  of  food  taking  that  I  have  observed  in 
a  large  number  of  cases  in  Amoeba  proteus  and  its  relatives.  The 
essential  points  are  the  sending  out  of  pseudopodia  on  each  side  of 
and  above  the  food  body  and  the  fusion  of  these  pseudopodia  at  their 
free  ends  or  edges,  thus  enclosing  the  food.  In  no  case,  in  these  species, 
was  there  any  evidence  that  the  Amoeba  was  aided  by  the  adherence 
of  the  food  body  to  its  protoplasm.  On  the  contrary,  there  was  a 
decided  tendency  for  the  food  body  to  be  pushed  away,  and  an  essential 
part  of  the  process  is  the  overcoming  of  this  mechanical  difficulty  by 
sending  out  a  pseudopodium  on  each  side  of  the  body  and  bending  the 
ends  of  them  together,  so  as  to  prevent  slipping  on  the  part  of  the 
food.*  That  this  difficulty  is  no  imaginary  one  will  be  shown  later, 
in  the  description  of  cases  where  the  Amoeba  was  unable,  after  many 
efforts,  to  enclose  the  food. 

It  is  commonly  said  that  the  posterior  rough,  tail-like  portion  of  the 
body  is  especially  important  in  the  taking  of  food,  though  it  is  sometimes 
added  that  one  rather  more  often  sees  the  partly  ingested  food  given  out 
again  in  this  region  (see  Leidy,  1879,  p.  45  ;  Penard,  1890,  p.  81  ;  1902, 
p.  16). t  I  have  never  seen  food  taken  in  at  this  part  of  the  body,  though, 
as  noted  above,  I  have  many  times  seen  it  taken  at  the  anterior  end. 
While  it  may  be  true  that  food  is  at  times  taken  at  the  posterior  end,  I 

♦This  lack  of  adherence  between  the  protoplasm  and  the  food  substance  is 
emphasized  by  Le  Dantec  (1894,  p.  68;  as  a  result  of  his  careful  studies  on  food- 
taking  in  Amoeba. 

tThe  references  to  food-taking  at  the  posterior  end  seem  all  to  go  back  to  a 
paper  by  P.  M.  Duncan,  "  Studies  amongst  Amoebae,"  in  the  Popular  Science 
Review  for  1877.     I  regret  that  I  have  been  unable  to  sec  this  paper. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  I95 

believe  that  the  supposed  prevalence  of  this  method  of  food-taking  and 
of  the  giving  off  of  incompletely  ingested  food  here  are  really  due  to 
incorrect  interpretation  of  another  very  common  process.  In  its  loco- 
motion Amoeba  frequently  comes  in  contact  with  diatoms,  desmids, 
encysted  Protozoa,  etc.  These  it  usually  creeps  over,  so  that  they  lie 
beneath  it.  As  the  Amoeba  progresses  the  objects  come  in  contact  w^ith 
the  posterior  portion  of  the  body,  w^hich  is  raised  from  the  bottom  and 
covered  with  a  viscid  secretion.  Owing  to  this  viscid  substance  the 
objects  often  cling  to  the  under  surface  of  this  part  of  the  body  and  are 
carried  along  with  it.  If  observed  at  this  time  one  cannot  tell  whether 
these  objects  have  been  ingested  or  not.  But  as  a  result  of  the  method 
of  movement  of  the  Amoeba  they  gradually  pass  to  the  posterior  end, 
and  are  usually  finally  left  behind.  When  such  an  object  separates  from 
the  Amoeba,  becoming  detached  from  its  under  surface,  it  appears  ex- 
actly as  if  it  were  given  off  from  within  ;  it  is  only  by  observing  the 
whole  process  from  beginning  to  end  that  one  can  be  sure  of  its  exact 
nature.  I  am  convinced  that  many  of  the  supposed  cases  of  the  inges- 
tion of  food  and  of  the  ejection  of  food  previously  ingested  at  the  poste- 
rior end  are  to  be  explained  in  this  way.  In  all  the  detailed  descriptions 
of  food-taking  in  forms  related  to  Afnoeba  proteus  that  I  have  found  in 
literature,  the  food  was  taken  at  the  anterior  end  in  a  way  similar  to 
that  which  I  have  described  above  (see  Carter,  1S63,  p.  45  ;  Wallich, 
1863,  c,  p.  453  ;  Leidy,  1879,  p.  49  ;  Le  Dantec,  1894,  p.  6%  ;  also  Biit- 
schli,  1880,  p.  117). 

In  Amoeba  verrucosa  and  the  other  species  which  do  not  often  form 
pseudopodia  food  is  taken  in  a  somewhat  different  manner.  Food- 
taking  in  Amoeba  verrucosa  has  been  described  by  Rhumbler  (1898, 
p.  205).  Penard  (1902),  though  he  spent  much  time  studying  this 
species,  says  that  he  has  not  observed  the  taking  of  food,  and  thinks  it 
must  occur  only  rarely.  In  my  own  cultures  specimens  of  this  species 
taking  food  were  positively  abundant.  I  have  seen  the  process  much 
oftener  than  in  other  species.  In  A.  verrucosa  and  its  relatives  food- 
taking  is  greatly  aided  by  the  tendency  of  foreign  particles  to  cling  to 
the  surface  of  the  body,  a  tendency  which  we  found  so  convenient  for 
determining  the  movement  of  points  on  the  body  surface  (see  pp.  140- 
146).  This  adhesiveness  of  the  outer  surface  compensates  for  the  lack  of 
formation  of  pseudopodia  in  these  species.  The  outer  surface  gradually 
sinks  in  at  the  point  where  the  food  body  is  attached  to  it.  The  latter 
is  thus  carried  to  the  inside  of  the  body,  surrounded  by  a  pouch  of 
ectosarc.  This  pouch  becomes  separated  from  the  outer  ectosarc.  The 
food  is  thus  completely  enveloped  and  later  digested.  Not  only  large 
objects,  but  often  very  small  ones,  spores  of  algae,  small  diatoms,  flagel- 
lates, etc.,  are  taken  in  in  this  way.      Rhumbler  (/.  c,  p.  20S)   has 


196 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


given  a  very  interesting  account  of  the  rolling  up  and  ingestion  of  threads 
of  Osciliaria  by  this  species  (see  p.  223).* 


PURSUIT   OF   FOOD. 


Amoeba  froteus  does  not  always  succeed  in  ingesting  its  food  so 
easily  as  in  the  case  just  described  (p.  194).  There  is,  as  noted  above, 
a  tendency  for  the  food  body  to  be  pushed  away  by  the  forward  move- 
ment at  the  anterior  end  of  the  Amoeba,  and  this  sometimes  gives 
serious  difficulty.  In  such  cases  Amceba  may  show  what  would  be 
called  in  higher  organisms  remarkable  pertinacity  in  continuing   its 


Fig.  73.t 

attempts  to  ingest  the  food.     This  will  be  illustrated  from  a  concrete 
case  (Fig.  73). 

An  Amoeba  froteus  was  creeping  toward  an  encysted  Euglena. 
The  latter  was  perfectly  spherical  and  very  easily  moved,  so  that  when 
the  anterior  edge  of  the  Amoeba  came  in  contact  with  it  the  cyst  merely 
moved  forward  a  little  and  slipped  to  one  side  (the  left).     The  Amoeba 


♦Leidy  C1879,  p.  86)  gives  a  very  similar  account  of  the  ingestion  of  filaments 
of  algae  in  Dinamoeba. 

tFiG.  73. — Amoeba  following  a  rolling  Euglena  cyst.  Nos.  1-9  shovr  successive 
positions  occupied  by  Amoeba  and  cyst.     See  text  for  explanation. 


I 


THE    MOVEMENTS    AND   REACTIONS   OF   AMCEBA.  I97 

thereupon  altered  its  course  so  as  to  follow  the  cyst  (Fig.  73,  i).  The 
cyst  was  shoved  forward  again  and  again,  a  little  to  the  left ;  the 
Amoeba  continued  to  follow.  This  continued  until  the  two  had  tra- 
versed about  one-fourth  the  circumference  of  a  circle  ;  then  (at  3)  the 
cyst,  when  pushed  forward,  rolled  to  the  left  quite  out  of  contact  with  the 
Amoeba.  The  latter  then  continued  forward  with  broad  anterior  edge 
in  a  direction  which  would  have  taken  it  past  the  cyst.  But  a  small 
pseudopodium  on  its  left  side  came  in  contact  with  the  cyst.  The 
Amoeba  thereupon  turned  again  and  followed  the  rolling  cyst.  At 
times  it  sent  out  two  pseudopodia,  one  on  each  side  of  the  cyst  (as  at 
4),  as  if  trying  to  inclose  the  latter,  but  the  ball-like  cyst  rolled  so  easily 
that  this  did  not  succeed.  At  other  times  a  single  very  long,  slender 
pseudopodium  was  sent  out,  only  the  tip  of  which  remained  in  contact 
with  the  cyst  (5).  Then  the  body  of  the  Amoeba  was  brought  up  from 
the  rear  and  the  cyst  pushed  farther.  This  continued  until  the  rolling 
cyst  and  the  following  Amoeba  had  described  almost  a  complete  circle, 
returning  nearly  to  the  point  where  the  Amoeba  had  first  come  in  con- 
tact with  the  cyst.  At  this  point,  owing  to  the  form  of  the  anterior 
end  of  the  Amoeba  (7)  the  cyst  rolled  to  the  right  instead  of  to  the  left 
as  it  was  pushed  forward.  The  Amoeba  followed  (8,  9).  This  new 
path  was  continued  for  two  or  three  times  the  length  of  the  Amoeba. 
The  direction  in  which  the  ball  was  rolling  would  soon  have  brought 
it  against  an  impediment,  and  I  thought  it  possible  that  the  Amoeba 
might  succeed  in  ingesting  it  after  all.  But  at  this  point  one  of  those 
troublesome  disturbers  of  the  peace  in  microscopic  work,  a  ciliate  infu- 
sorian,  came  near  and  whisked  the  ball  away  in  its  ciliary  current. 
After  the  ball  was  carried  away  the  Amoeba  continued  to  follow  in  the 
same  direction  for  only  a  very  short  distance,  about  one-fifth  its  length, 
then  reversed  its  course  and  went  elsewhere. 

The  movements  of  Amoeba  are,  of  course,  very  slow,  and  the  behavior 
described  required  a  considerable  period  of  time — 10  or  15  minutes,  I 
should  judge.  The  whole  scene  made  really  an  extraordinary  impres- 
sion on  the  observer,  and  it  is  diflScult  in  describing  it  to  refrain  from 
the  use  of  words  that  imply  a  great  deal  of  resemblance  between  Amoeba 
and  immensely  higher  organisms.  One  seems  to  see  that  the  Amoeba  is 
trying  to  obtain  this  cyst  for  food,  that  it  puts  forth  efforts  to  accom- 
plish this  in  various  ways,  and  that  it  shows  remarkable  pertinacity 
in  continuing  its  attempts  to  ingest  the  food  when  it  meets  with  diffi- 
culty. Indeed,  the  scene  could  be  described  in  a  much  more  vivid 
and  interesting  way  by  the  use  of  terms  still  more  anthromorphic  in 
tendency. 

I  have  seen  a  large  number  of  cases  like  that  above  described ;  in 
some  of  my  cultures  containing  many  specimens  of  Amoeba  proteus 


98 


THK  BEHAVIOR  OF  LOWKR  ORGANISMS. 


and  many  Euglena  cysts  it  was  not  at  all  rare  to  find  the  animals 
engaged  in  thus  following  a  rolling  ball  of  food.  I  have  made  full 
notes  and  sketches  of  a  number  of  other  cases,  but  they  show  nothing 
diflferent  in  principle  from  that  above  described,  so  that  it  is  not  worth 
while  to  enter  into  details.  One  further  point  is,  however,  worthy  of 
special  note.  Often  a  single  pseudopodium  comes  in  contact  with  such 
a  cyst  and  stretches  out  toward  it,  while  the  remainder  of  the  Amoeba 
continues  on  its  course,  away  from  the  cyst.  The  pseudopodium  in 
contact  then  stretches  out  as  far  as  possible,  keeping  in  contact  with 
the  cyst  and  often  pushing  it  ahead  (Fig.  74)1  until  it  is  finally  pulled 
bodily  away  by  the  movements  of  the  whole  Amoeba.  Apparently  this 
one  pseudopodium  reacts  to  the  stimulus  quite  independently  of  the 
remainder  of  the  body.  Again,  two  pseudopodia  on  opposite  sides  of 
the  body  may  each  come  in  contact  with  a  cyst.     Each  then  stretches 


Fig.  74.* 

out,  pulling  a  portion  of  the  body  with  it,  and  follows  its  cyst,  until  the 
body  forms  two  lobes,  connected  only  by  a  narrow  isthmus.  Finally, 
one  half  succeeds  in  pulling  the  other  away  from  the  attachment  to  the 
substratum,  and  the  entire  Amoeba  follows  the  victorious  pseudopodium. 
Mechanical  stimuli  are,  of  course,  involved  in  the  above  reactions ; 
perhaps  also  chemical  stimuli  from  the  cyst.  It  is  important  from  the 
theoretical  standpoint  to  note  that  the  movement  of  particles  on  the 
surface  of  the  Amoeba  is  toward  the  object  causing  the  reaction.  This 
I  have  been  so  fortunate  as  to  have  opportunity  of  observing  in  several 
cases. 

OTHER    AMCEB^    AS    FOOD. 

Amoebae  frequently  prey  upon  each  other,  as  Leidy  has  already  de- 
scribed and  figured  (1879,  p.  94;  plate  7,  Figs.  12-19).  ^^t  the  victim 
does  not  always  conduct  itself  so  passively  as  in  the  case  described  by 
Leidy,  and  sometimes  finally  escapes  from  its  pursuer.     A  description 

♦Fig.  74. — A  single  pseudopodium  {x)  reacts  positively  to  a  Euglena  cyst,  the 
protoplasm  flowing  in  direction  of  cjst  and  pushing  it  forward,  while  remainder 
of  the  Amoeba  moves  in  another  direction  ;  1—4,  successive  forms  taken.  At  4  the 
reacting  pseudopodium  is  pulled  awaj  from  the  cjst,  and  then  contracts. 


THE   MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


199 


of  two  or  three  concrete  cases  among  those  which  I  have  observed  in 
Amoeba  angulata  will  bring  out  the  nature  of  the  behavior  under  such 
conditions.  Penard  (1902,  p.  700)  mentions  that  he  has  seen  one 
Amoeba  pursue  and  finally  capture  another,  but  does  not  give  a  detailed 
account  of  the  process. 

(i)  Two  Amoebae  were  observed,  a  large  one  and  a  small  one,  the 
former  apparently  attempting  to  swallow  the  latter  (Fig.  "j^^).  The 
small  Amoeba  was  creeping  rapidly  forward,  while  its  wrinkled  pos- 
terior portion  was  enveloped  by  the  anterior  part  of  the  larger  Amoeba. 
The  large  Amoeba  had  the  anterior  portion  of  its  body  quite  hollowed 
out,  so   as  to  form  a  cavity  large  enough  to  contain  the  entire  small 

1 _ 

2 


Fig.  75.* 

Amoeba,  and  in  the  anterior  portion  of  this  cavity  was  inclosed  the 
hinder  portion  of  the  body  of  the  smaller  Amoeba.  Whether  this 
cavity  was  bounded  below  as  well  as  above  and  at  the  sides  by  pro- 
toplasm I  could  not  determine  with  certainty.  The  large  Amoeba  was 
following  the  small  one,  moving  at  about  the  same  rate.  There  was 
no  union  between  the  protoplasm  of  the  two ;  on  the  contrary  the 
boundaries  of  both  were  clearly  defined,  and  they  seemed  to  be  only 
slightly  in  contact,  the  posterior  end  of  the  small  specimen  moving 
easily  within  the  cavity  of  the  other.  As  they  moved  forward,  some- 
times the  posterior  specimen  flowed  a  little  faster,  and  then  a  little 
more  of  the  smaller  one  became  enveloped ;  at  other  times  the  smaller 
Amoeba  moved  a  little  faster,  and  then  withdrew  a  part  of  its  inclosed 


*  Fig.  75. — Pursuit  of  one  Amoeba  by  another.     See  text  for  explanation. 


200  THE    BEHAVIOR    OF    LOWFiR    ORGANISMS. 

tail.  They  proo^ressed  in  this  fashion  for  a  long  distance,  many  times 
their  own  length.  I  watched  them  thus  for  more  than  lo  minutes. 
The  smaller,  anterior  specimen  frequently  altered  its  course ;  the 
posterior  one  followed.  T  stimulated  the  anterior  end  of  the  small 
specimen  with  the  tip  of  a  glass  rod  (Fig.  75,  3) ;  it  turned  at  a  right 
angle,  and  the  posterior  specimen  followed.  After  about  12  minutes  it 
could  be  seen  that  the  smaller  specimen  was  moving  slightly  faster 
than  the  other  and  was  slowly  withdrawing  its  posterior  end.  Finally 
it  pulled  completely  away  from  the  large  Amoeba,  which  was  still  fol- 
lowing as  rapidly  as  possible.  After  the  small  Amoeba  had  completely 
escaped  the  large  one  stopped  and  remained  entirely  quiet  for  a  few 
seconds.  The  large  cavity  in  its  anterior  portion,  which  it  had  pre- 
pared for  the  reception  of  the  small  Amoeba,  and  which  extended 
back  behind  the  middle  of  the  body,  was  still  very  evident.  After  a 
time  the  Amoeba  began  to  change  form  and  sent  out  pseudopodia 
irregularly  in  all  directions.  The  smaller  Amoeba  continued  its  for- 
ward locomotion  as  long  as  observed.  The  performance  is  illustrated 
in  Fig.  75,  from  sketches  made  while  it  was  in  progress. 

(2)  In  a  second  case  I  was  able  to  observe  the  beginning  as  well  as 
the  end  of  this  microscopical  drama  (Fig.  76).  I  had  attempted  to 
cut  an  Amoeba  in  two  with  the  tip  of  a  glass  rod,  in  the  manner  described 
later.  The  posterior  third  of  the  Amoeba,  in  the  form  of  a  wrinkled 
ball,  remained  attached  to  the  body  only  by  a  slender  cord,  the  remains 
of  the  ectosarc.  The  Amoeba  began  to  creep  away,  dragging  with  it 
this  ball.  I  will  call  this  Amoeba  a^  while  the  ball  will  be  designated  b. 
A  larger  Amoeba  {c)  approached,  moving  at  right  angles  to  the  path 
of  the  first  Amoeba ;  its  course  accidentally  brought  it  into  contact 
with  the  ball  /$,  which  was  dragging  past  its  front.  Amoeba  c  there- 
upon turned,  followed  Amoeba  a,  and  began  to  engulf  the  ball  b,  A 
large  cavity  was  formed  in  the  anterior  end  of  Amoeba  c,  reaching  back 
nearly  or  quite  to  its  middle,  and  much  more  than  sufficient  to  contain 
the  ball  b.  Amoeba  a  now  turned  into  a  new  path  ;  Amoeba  c  followed 
(Fig.  76  at  4) .  After  the  pursuit  had  lasted  for  some  time  the  ball  b 
had  become  completely  enveloped  by  Amoeba  c;  the  cord  connecting 
it  with  Amoeba  a  broke,  and  the  latter  went  on  its  way  (at  5)  and  dis- 
appears from  our  account.  Now  the  anterior  opening  of  the  cavity  in 
Amoeba  c  became  partly  closed,  leaving  a  slender  canal  (5) .  The  ball  b 
was  thus  completely  inclosed,  together  with  a  quantity  of  water. 
There  was  no  union  or  adhesion  of  the  protoplasm  of  b  and  c;  on  the 
contrary  (as  the  sequel  will  show  clearly)  both  remained  quite  sepa- 
rate, c  merely  inclosing  b. 

Now  the  large  Amoeba  c  stopped,  then  began  to  move  in  another 
direction  (Fig.  76,  5-6),  carrying  with  it  its  meal.     But  the  meal,  the 


THE    MOVEMENTS    AND    REACTIONS   OF   AMCEBA. 


20I 


ball  3,  now  began  to  show  signs  of  life,  sent  out  pseudopodia,  and, 
indeed,  became  very  active.  We  shall  henceforth,  therefore,  speak  of  it 
as  Amoeba  b.  It  began  to  creep  out  through  the  still  open  canal,  send- 
ing forth  its  pseudopodia  to  the  outside  (Fig.  76,  7).  Thereupon 
Amoeba  c  sent  forth  its  pseudopodia  in  the  same  direction,  and  after 
creeping  in  that  direction  several  times  its  own  length,  again  completely 


Fig.  76.* 

inclosed  b  (7-8).  The  latter  again  partly  escaped  (9),  and  was  again 
engulfed  completely  (10).  Amoeba  c  now  started  again  in  the  opposite 
direction  (i  i),  whereupon  Amoeba  3,  by  a  few  rapid  movements,  escaped 
entirely  from  the  posterior  end  of  c,  and  was  free,  being  completely 
separated  from  c  (11-12).  Thereupon  c  reversed  its  course  (12),  crept 
up  to  3,  engulfed  it  completely  again  (13),  and  started  away.    Amoeba  b 


*FiG.  76. — Pursuit,  capture,  and  ingestion  of  one  Amoeba  bv  another;  escape 
of  captured  AmcBba  and  its  recapture ;  final  escape.    See  text  for  detailed  account. 


202  THE  BEHAVIOR  OF  LOWER  ORGANISMS. 

now  contracted  into  a  ball,  its  protoplasm  clearly  set  off  from  the  pro- 
toplasm of  its  captor,  and  remained  quiet  for  a  time.  Appai'ently  the 
drama  was  over.  Amoeba  c  went  on  its  way  for  about  five  minutes, 
without  any  sign  of  life  in  b.  In  the  movements  of  the  Amoeba  c  the 
ball  b  gradually  became  transferred  to  the  posterior  end  of  c,  until 
finally  there  was  only  a  thin  layer  between  b  and  the  outer  water. 
Now  b  began  to  move  again,  sent  out  pseudopodia  to  the  outside 
through  the  thin  wall,  and  then  passed  bodily  out  into  the  water  (14). 
This  time  Amoeba  c  did  not  return  and  recapture  b.  The  two  Amoebse 
moved  in  different  directions  and  remained  completely  separated.  The 
whole  performance  occupied,  I  should  judge,  about  12  to  15  minutes 
(the  time  was  not  taken  till  several  minutes  after  the  beginning). 

After  working  with  simple  stimuli  and  getting  always  direct  simple 
responses,  so  that  one  begins  to  feel  that  he  understands  the  behavior 
of  the  animal,  it  is  somewhat  bewildering  to  become  a  spectator  of  so 
striking  and  complicated  a  drama.  If  we  attempt  an  analysis  of  the 
observed  behavior  of  the  Amoeba  c  into  stimuli  and  reactions,  we  ob- 
tain some  such  a  result  as  follows  :  At  first  the  stimulus  of  contact  with 
^,  and  perhaps  a  chemical  stimulus  from  the  same  source,  causes  the 
Amoeba  c  to  react  by  flowing  toward  ^,  and  at  the  same  time  to  change 
form,  so  as  to  hollow  out  the  anterior  end.  Later,  every  change  in  the 
direction  of  movement  of  a  and  b  induces  a  corresponding  change  in 
the  direction  of  movement  of  c/  there  is  a  finely  co-ordinated  adapta- 
tion of  the  latter  to  the  movements  of  the  former.  After  the  separation 
of  b  from  ^,  the  movement  of  c  (at  5-6)  in  a  different  direction  may 
have  been  due  to  some  external  stimulus.  But  what  is  the  stimulus  for 
the  change  of  direction  of  locomotion  in  the  Amoeba  c  at  7  when  b  has 
begun  to  escape  .''  And  why  does  Amoeba  c  go  in  that  direction  only 
long  enough  to  get  b  firmly  inclosed  again,  then  reverse  its  course  .^^ 
And,  finally,  why  does  Amoeba  c  reverse  its  course  at  1 1-13,  when  b  has 
entirely  escaped,  and  continue  in  this  reversed  direction  till  it  reaches 
and  recaptures  b?  The  action  is  remarkably  like  that  of  a  higher 
animal.  Doubtless  we  must  assume  chemical  and  mechanical  stimuli 
as  directives  for  each  of  the  movements  of  c,  but  the  analysis  so  obtained 
seems  not  very  complete  or  satisfactory. 

REACTIONS    TO   INJURIES. 

Certain  cases  that  belong  under  the  heading  of  reactions  to  injuries 
have  already  been  described  as  evidences  of  the  contractility  of  the 
ectosarc;  for  these  page  180  should  be  consulted.  The  cases  which 
we  take  up  here  are  of  a  different  character.  They  concern  Amoeba 
angulaia. 

Jensen  (1896)  has  shown  in  the  case  of  certain  Foraminifera  that 
two  pieces  of  protoplasm  from  the  same  individual  will  readily  unite 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA. 


JO3 


if  brought  in  contact,  while  pieces  from  different  individuals  will  not 
thus  unite.  I  was  interested  in  the  question  as  to  whether  this  would 
hold  true  also  for  Amoeba,  and  for  that  purpose  undertook  to  cut  speci- 
mens in  two.  With  the  fine  tip  of  a  glass  rod  it  is  possible,  under  the 
microscope,  in  the  open  drop,  to  cut  in  two  an  elongated  Amoeba  at 
almost  any  desired  point.  The  sharp  point  of  the  rod  is  simply  drawn 
across  the  Amoeba  as  it  lies  outspread  on  the  substratum. 

In  this  operation  it  was  found  that  the  Amoeba  was  not,  as  a  rule,  at 
first  completely  cut  in  two  by  the  stroke  itself.  The  endosarc  is  divided 
completely,  but  the  two  halves  are  still  connected  by  a  thin  layer  of 
ectosarc,  which  resists  the  cutting,  and  shows  fine  longitudinal  stria- 
tions ;  these  may  be  merely  longitudinal  folds  (Fig.  77,  2).  This  thin 
layer  of  ectosarc  seems  very  tenacious. 


Fig.  77.* 

The  Amoeba  is  thus  left  in  the  condition  shown  in  Fig.  77,  2.  The 
two  halves  usually  both  contract  strongly.  Now  ensues  a  very  pecu- 
liar process.  One  of  the  two  halves  begins  to  send  out  pseudopodia 
in  such  a  way  as  to  partly  inclose  the  other  (3) ;  the  second  half  is 
thus  drawn  as  a  narrow  wedge-shaped  mass  inside  of  the  other,  as  at  4. 
It  seems  to  be  usually  the  half  that  contains  the  nucleus  that  envelopes 
the  other,  though,  as  will  be  shown  later,  the  nucleus  is  not  necessary 
for  this  reaction.  If  the  piece  thus  embraced  is  considerably  smaller 
than  the  other,  it  may  become  completely  inclosed,  and  is  then  carried 
away,  appearing  like  a  mass  of  food.  It  does  not  become  fused  with 
the  remainder  of  the  protoplasm,  but  there  is  a  sharp  boundary  between 
it  and  that  which  envelopes  it.  Specimens  were  followed  for  10  min- 
utes after  thus  inclosing  a  piece  of  their  own  bodies ;  during  this  time 
no  marked  change  was  seen  to  occur  in  the  inclosed  piece. 

In  the  much  more  common  cases  where  the  two  pieces  are  nearly 


204  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

equal  in  size,  or  when  it  is  the  smaller  piece  that  begins  to  envelop 
the  larger,  the  process  results  differently.  After  one  piece  has  been 
drawn  far  into  the  other  (Fig.  77,  4),  both  seem  to  contract  strongly, 
whereupon  the  connecting  band  of  ectosarc  breaks,  the  partly  inclosed 
piece  is  squeezed  out  of  the  other ;  and  the  two  separate.  Usually 
each  retains  its  form  for  a  few  seconds  after  separation  ;  one  bearing 
a  slender  truncate  pyramid  or  cone,  while  the  other  shows  a  deep 
depression  corresponding  to  this  pyramid  (Fig  77,  5).  After  a  time 
both  halves  change  form  and  move  away.  Usually  the  half  which 
partly  inclosed  the  other  becomes  active  long  before  the  other,  but 
this  is  not  invariably  true. 

In  a  large  number  of  cases  observed  it  was  the  part  which  contained 
the  nucleus  that  attempted  to  envelop  the  other  half.  In  order  to 
determine  whether  the  nucleus  plays  a  necessary  part  in  this  perform- 
ance, I  tried  the  following  experiment:  After  the  half  which  had 
no  nucleus  had  again  become  active  and  was  moving  about,  I  cut  it  in 
two,  as  before.  Now  one  half  of  this  piece  partly  enveloped  the  other 
in  the  usual  way,  thus  showing  that  the  nucleus  is  not  necessary  for 
this  reaction. 

These  results  should  be  compared  with  Penard's  observations  on 
injured  specimens  of  A,  terricola^  noted  on  page  180  of  the  present 
paper. 

As  to  the  question  which  these  experiments  were  originally  intended 
to  answer,  whether  two  pieces  of  a  single  Amoeba  would  reunite 
after  separation,  my  results  were  negative.  After  the  two  pieces  had 
begun  to  move  about  freely  they  were  induced  to  come  in  contact,  or 
sometimes  they  came  in  contact  accidentally  ;  but  in  no  case  was  there 
any  union.  Prowazek  (1901,  p.  93)  obtained  the  same  result  with 
small  species  of  Amoeba,  but  in  a  larger  undetermined  species  he  suc- 
ceeded in  bringing  about  a  union  of  pieces  not  only  from  the  same 
individual,  but  from  different  individuals. 

PHYSICAL  THEORIES  AND  PHYSICAL  IMITATIONS  OF 
AMCEBOID  MOVEMENTS. 

THE    SURFACE    TENSION   THEORY. 

The  movements  of  Amoeba  as  presented  by  Biitschli  (18S0,  1893) 
and  Rhumbler  (1S98)  (see  Figs.  30-33)  are  exactly  those  of  a  drop  of 
fluid  moving  as  a  result  of  a  local  change  in  surface  tension  (Fig.  34). 
It  was,  therefore,  natural  to  assume  that  the  cause  of  the  movements  is 
the  same  in  the  two  cases.  This  is  the  view  taken  by  the  two  authors 
named.  According  to  Biitschli,  Rhumbler,  and  many  other  authors, 
Amoeba  is  a  drop  of  complex  fluid  which  moves  about  as  a  result  of 
local  changes  in  surface  tension. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  205 

In  the  foregoing  investigation  it  has  been  shown  that  the  movements 
in  Amoeba  are  not  of  the  character  supposed  by  Biitschli  and  Rhumbler. 
There  is,  indeed,  very  little  resemblance  betw^een  the  movements  of 
Amoeba  and  those  of  an  inorganic  drop  moving  as  a  result  of  a  local 
change  in  surface  tension.  The  difference  is  clearly  brought  out  by  a 
comparison  of  Fig.  58,  showing  the  currents  in  Amoeba,  with  Fig.  34, 
showing  those  in  the  inorganic  drop.  The  more  striking  differences 
are  as  follows : 

(i)  In  the  drop  moving  as  a  result  of  a  local  change  in  surface  ten- 
sion the  currents  on  the  surface  are  (and  must  be)  away  from  the  side 
on  which  a  projection  is  formed  and  toward  which  the  drop  is  moving ; 
in  the  Amoeba  the  surface  current  is  toward  this  side. 

(2)  In  the  drop  the  surface  currents  are  in  a  direction  opposed  to 
that  of  the  axial  current ;  in  Amoeba  surface  currents  and  axial  current 
are  in  the  same  direction. 

(3)  The  movement  of  Amoeba  is  in  the  nature  of  rolling,  the  upper 
surface  passing  continually  around  the  anterior  end  and  becoming  the 
lower  surface.  In  the  inorganic  drop  there  is  no  such  rolling  move- 
ment, but  the  interior  portions  of  the  fluid  are  continually  passing  to 
the  surface  at  the  anterior  end. 

Clearly,  then,  the  forces  producing  the  movements  in  the  two  cases 
are  not  acting  in  the  same  manner.  The  locomotion  of  Amoeba  is 
demonstrably  not  due  to  a  local  decrease  in  surface  tension  on  the  side 
toward  which  the  animal  is  moving. 

This  becomes  still  clearer  when  we  consider  in  detail  the  method  by 
which  the  movements  are  produced  in  a  drop  of  inorganic  fluid  as  a 
result  of  a  local  decrease  in  its  surface  tension. 

The  phenomena  of  surface  tension  are  usually  considered  to  be  the 
result  of  the  uncompensated  attractions  of  those  particles  of  the  fluid 
which  are  near  to  the  surface.  Such  particles  are  attracted  inward  and 
laterally,  but  not  outward  (or  less  strongly  outward) .  The  resulting 
forces  may  be  considered  as  resolvable  into  two  components,  one  acting 
tangent  to  the  surface,  the  other  acting  perpendicular  to  the  surface. 
The  former  is  what  may  be  called  surface  tension  proper ;  the  latter 
is  often  spoken  of  as  normal  pressure.  The  result  is  very  much  as  if 
the  fluid  were  covered  with  a  stretched  India  rubber  membrane. 
These  relations  are  well  set  forth  in  a  recent  paper  of  Jensen  (1901). 
It  is  further  to  be  noted  that  these  two  components,  surface  tension  and 
normal  pressure,  are  two  aspects  of  one  and  the  same  thing,  and,  there- 
fore, vary  together  and  from  the  same  causes  ;  they  can  not  be  separated 
either  theoretically  or  experimentally.  Whenever  one  of  these  factors 
increases  or  decreases,  the  other  shows  a  corresponding  change.  The 
two  are  often  spoken  of  (together  with  the  pressure  due  to  curvature  of 
the  surface)  as  surface  tension  (see  Jensen,  /.  c). 


2o6  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Now,  when  the  interattraction  of  the  particles  at  a  certain  region  of 
the  surface  of  a  mass  of  fluid  is  decreased,  the  pressure  inward  and  the 
tension  along  the  surface  are  decreased.  As  the  pressure  remains  the 
same  elsewhere,  fluid  tends  to  be  pressed  out  at  the  point  where  the 
pressure  is  lowered  ;  thus  a  projection  may  be  formed  here.  As  the 
tension  remains  the  same  elsewhere,  the  remainder  of  the  surface  of 
the  drop  pulls  harder  than  that  of  the  region  under  consideration  ; 
hence  it  pulls  the  surface  of  the  fluid  away  from  the  region  where  the 
tension  is  lowered.  The  effect  is  similar  to  that  which  would  be 
produced  if  one  portion  of  a  stretched  sheet  of  India  rubber  w^ere 
weakened  or  cut ;  the  remainder  of  the  sheet  would  pull  away  from  this 
region.  Thus  there  are  produced  the  currents  characteristic  of  such  a 
drop  of  fluid — an  axial  current  toward  the  region  of  lowered  tension, 
surface  currents  away  from  the  region  of  lowered  tension  (Fig.  34). 
An  increase  in  the  tension  at  the  opposite  side  would  produce  exactly 
the  same  currents,  as  Rhumbler  (1898,  p.  188)  has  set  forth,  the  axial 
current  being  always  toward  the  region  of  lowest  tension,  the  surface 
currents  in  the  opposite  direction. 

In  the  moving  Amoeba,  as  we  have  seen,  the  currents  are  by  no 
means  of  this  character.  The  axial  current  and  the  surface  current  are 
congruent,  and  both  are  in  the  direction  of  locomotion.  Such  move- 
ment could  not  be  produced  by  a  local  decrease  in  the  surface  tension 
of  some  part  of  the  body  surface. 

The  formation  of  pseudopodia  is,  as  we  have  seen,  essentially  the 
same  process  as  the  forward  movement  at  the  anterior  end  of  the 
AmcEba.  On  the  upper  surface  of  a  pseudopodium  that  is  in  contact 
with  the  substratum  there  is  a  forward  movement,  so  that  particles 
clinging  to  the  upper  surface  are  carried  over  the  tip ;  the  currents 
which  must  result  from  a  decrease  in  surface  tension  are  not  present. 
On  the  contrary,  there  is  a  current  on  the  surface  in  the  opposite  direc- 
tion from  that  required.  The  formation  of  such  a  pseudopodium  can 
not,  then,  be  due  to  a  local  decrease  in  surface  tension. 

The  same  is  true,  essentially,  when  a  pseudopodium  is  sent  out  into 
the  water,  not  coming  in  contact  with  a  surface.  In  such  a  case,  as 
we  have  seen,  the  entire  surface  moves  outward,  in  the  same  direction 
as  the  tip  ;  there  is  no  such  backward  movement  as  the  theory  requires. 

Altogether,  it  is  clear  that  the  supposed  resemblance  between  the 
movements  and  internal  currents  of  Amoeba  and  those  of  a  drop  of  fluid 
moving  as  a  result  of  a  local  increase  or  decrease  of  surface  tension 
does  not  exist.  We  must  conclude  that  the  movements  of  Amoeba  are 
not  due  to  local  changes  in  surface  tension. 

One  might  be  tempted  to  inquire  whether  the  movement  of  Amoeba 
could  not  be  explained  by  considering  separately  the  action  of  the  two 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  207 

factors  in  surface  tension,  the  "surface  tension  proper"  and  the 
"  normal  pressure."  If  the  normal  pressure,  directed  inward,  were 
decreased  in  a  certain  region,  while  the  tangential  factor,  the  "surface 
tension  proper,"  were  not  decreased,  were  perhaps  even  increased, 
could  not  pseudopodia  be  formed  as  actually  occurs,  without  any  back- 
ward current  on  the  surface  ?  Jensen  seems  to  lean  toward  the  possi- 
bility of  such  action  when  he  speaks  of  the  variation  of  one  of  these 
factors  without  the  other  (Jensen  1901,  p.  374).* 

But  with  such  an  inquiry  should  we  hot  leave  the  field  of  realities  to 
wander  among  abstractions  ?  One  who  is  not  a  physicist  can,  of  course, 
not  speak  positively  on  such  a  point.  Yet,  so  far  as  I  am  able  to  dis- 
cover from  the  results  of  experiments  and  from  the  theories  of  surface 
tension,  the  state  of  the  case  is  about  as  follows  :  The  tangential  tension 
and  the  normal  pressure  are  not  two  different  things ;  they  are  only 
different  aspects  of  one  and  the  same  thing.  Viewed  from  the  stand- 
point of  "  energetics,"  what  the  physical  experiments  show  liquids  to 
possess  is  surface  energy,  in  virtue  of  which  they  tend  to  decrease  their 
surface  and  resist  an  increase  of  surface,  however  these  changes  are 
brought  about  (see  Ostwald,  1902,  p.  197).  When  the  "  surface  ten- 
sion is  decreased  "  in  a  certain  region  {x)  of  a  fluid  mass,  this  signifies  that 
the  tendency  to  a  decrease  of  surface  and  the  resistance  to  an  increase 
of  surface  is  lessened  in  this  region.  As  a  result,  the  remainder  (j/)  of 
the  fluid  decreases  its  surface  at  the  expense  of  the  region  x;  the  latter 
is  thus  compelled  to  increase  its  surface.  This  takes  place  by  simulta- 
neous passage  of  the  contents  of  y  into  x  and  of  the  surface  of  at  on  to 
y,  the  two  operations  being  essentially  one,  and  both  having  the  result 
of  decreasing  the  surface  of  y  and  increasing  that  of  x.  There  would 
seem  to  be  no  ground,  theoretical  or  experimental,  for  supposing  that 
in  a  fluid  one  of  these  operations  could  take  place  without  the  other. 
An  attempted  explanation  of  this  sort  would  be,  if  these  considerations 
are  correct,  not  a  physical  explanation,  but  a  purely  hypothetical  one, 
working  with  conditions  not  known  to  exist.  The  whole  value  of  the 
surface  tension  theory  lies  in  its  direct  reference  back  to  the  results 
of  physical  experiments — in  its  fidelity  to  the  results  of  such  experi- 
ments. As  soon  as  it  leaves  this  ground  it  becomes  of  no  more  value 
than  the  thousand  and  one  other  hypotheses  that  have  been  constructed 
for  the  explanation  of  contractility. 

Further,  even  this  purely  hypothetical  explanation  could  not  account 
for  the  forward  currents  on  the  upper  surface  of  Amoeba,  nor  for  the 
transference  of  portions  of  the  body  surface  to  the  surface  of  a  pseudo- 
podium.  In  any  form  we  can  give  it,  the  theory  that  the  movement  is 
due  to  local  changes  in  surface  tension  is  not  in  agreement  with  the 
observed  phenomena. 

*  Though  elsewhere  he  speaks  of  the  necessity  of  their  varying  together. 


J08  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

BERTHOLD's     THEORY    THAT     ONE-SIDED     ADHERENCE    TO     THE     SUB- 
STRATUM   IS    THE   CAUSE    OF   LOCOMOTION. 

If,  then,  the  movements  of  Amoeba  are  not  due  to  local  decrease  in  sur- 
face tension,  with  the  formation  of  *'Ausbreitungscentren  "  (Biitschli), 
is  it  possible  to  find  a  physical  explanation  for  them  ?  In  taking  up 
this  question  we  must  consider  separately  (i)  locomotion,  and  (2)  the 
formation  of  pseudopodia. 

Observation  and  experiment  indicate,  as  we  have  seen  in  the  obser- 
vational portion  of  this  paper,  that  Amoeba  is  a  drop  of  fluid  which 
becomes  attached  to  the  substratum  in  front  and  pulls  itself  forward, 
the  pull  extending  backward  from  the  attached  region  over  the  upper 
surface,  and  producing  a  rolling  motion. 

Now,  a  drop  of  inorganic  fluid  under  the  influence  of  similar 
forces  moves  in  precisely  the  same  manner.  There  is  no  great  difli- 
culty  in  causing  a  drop  of  inorganic  fluid  to  adhere  more  strongly  to 
the  substratum  on  one  side  than  elsewhere.  When  this  is  brought 
about  the  drop  moves  toward  the  more  adherent  side  by  a  rolling 
motion,  precisely  like  that  of  Amoeba.  By  a  proper  arrangement  of 
the  conditions  almost  every  detail  of  amoeboid  locomotion  may  be 
closely  imitated. 

That  this  is  the  method  of  movement  in  Amoeba  was  the  theory 
maintained  by  Berthold  (1886),  though  it  is  rather  curious  that  the 
supposed  facts  on  which  he  based  this  view  were  incorrect.  Berthold 
confirmed  on  the  basis  of  observations  on  A?noeba  verrucosa  (  !  )  and 
other  species  the  account  of  the  currents  in  Amoeba  given  by  Schulze 
(see  p.  137  and  Fig.  37)  ;  that  is,  such  currents  as  would  be  consistent 
with  the  theory  of  local  decrease  in  surface  tension,  but  are  quite  incon- 
sistent with  his  own  theory.  He  rejected  the  theory  that  locomotion  is 
due  to  a  decrease  in  surface  tension  at  the  anterior  end,  on  the  ground 
that  no  currents  are  to  be  observed  in  the  surrounding  water,  as  this 
theory  demands.  Berthold  held  that  the  locomotion  is  due  to  the 
spreading  out  of  the  anterior  end  of  the  fluid  mass  on  the  surface  of  a 
solid,  this  spreading  out  being  due  to  adhesion  between  the  fluid  and 
the  solid.  Unfortunately  for  the  understanding  of  his  theory,  he  tried 
to  bring  this  into  relation  with  many  other  much  less  simple  phenom- 
ena. In  particular  he  compared  the  movements  to  those  of  a  drop  of 
water  on  a  glass  plate,  which  flees  when  a  rod  wet  with  ether  is  brought 
near  one  side.  This  was  an  unfortunate  comparison,  as  the  movements 
in  a  drop  of  water  under  such  circumstances  are  of  a  character  entirely 
different  from  those  produced  when  a  mass  of  fluid  adheres  by  one  side 
to  a  solid.  The  movement  in  a  drop  of  water  fleeing  from  the  ether- 
ized rod  is  a  result  of  the  currents  produced  by  the   lowering  of  the 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  2O9 

surface  tension  on  one  side,  as  Biitschli  (1892,  pp.  191  and  194),  has 
shown.  This  comparison,  and  Berthold's  discussion  of  the  relations 
between  spreading  out  on  the  surface  of  solids  and  on  the  surface  of 
liquids,  together  with  his  incorrect  idea  of  the  currents  in  such  spread- 
ing out  on  a  solid,  have  served  to  distract  the  attention  of  investigators 
from  the  really  simple  essential  features  of  such  a  theory.  Berthold 
did  not  attempt  to  study  directly  the  currents  and  other  movements  of 
a  drop  of  fluid  moving  as  a  result  of  one-sided  adherence  to  a  solid. 
We  may,  therefore,  leave  his  account  and  examine  for  ourselves  the 
phenomena  in  question. 

EXPERIMENTAL    IMITATION   OF   THE    LOCOMOTION    OF   AMCEBA. 

The  experiments  with  inorganic  fluids  may  be  performed  as  follows  : 
A  piece  of  smooth  cardboard,  such  as  the  Bristol  board  used  for  drawing, 
is  placed  on  the  level  bottom  of  a  shallow  vessel,  such  as  a  Petrie  dish, 
and  soaked  with  bone  oil  by  spreading  the  latter  over  its  surface.  A 
small  area  on  the  surface  of  the  board  is  protected  from  the  oil  by 
placing  upon  it  a  drop  of  water.  After  the  board  has  become  well 
soaked,  the  drop  of  water  is  removed  with  a  pipette,  leaving  this  spot 
merely  damp,  while  a  layer  of  oil  some  millimeters  deep  is  poured  into 
the  vessel,  covering  the  cardboard  completely.  A  drop  of  glycerine  or 
of  water  is  then  introduced;  this  settles  to  the  bottom,  but  adheres  to 
it  only  slightly.  A  drop  of  glycerine  is  in  some  respects  preferable,  as 
its  movements  are  slower.  To  the  drop  should  be  added  beforehand  a 
quantity  of  soot,  in  order  to  make  its  internal  movements  visible. 
Some  of  the  soot  remains  on  the  surface,  projecting  out  into  the  oil, 
thus  making  it  possible  to  observe  the  surface  currents. 

If  the  drop  is  brought  close  to  the  spot  on  the  cardboard  that  was 
protected  from  the  oil,  so  that  one  side  comes  in  contact  with  this 
region,  the  edge  of  the  glycerine  or  water  drop  spreads  out  over  this 
area.  Thereupon  the  remainder  of  the  drop  is  pulled  in  that  direction, 
till  the  whole  drop  takes  up  its  position  over  the  protected  spot.  In 
the  movement  of  the  drop  toward  the  area  to  which  one  side  adheres, 
it  rolls  exactly  as  Amoeba  does.  The  currents  on  the  upper  surface 
and  within  the  drop  are  forward.  Toward  the  sides  the  currents  are 
somewhat  less  marked,  and  on  the  under  surface  they  cease  entirely ; 
particles  within  the  drop  but  in  contact  with  the  lower  surface  are  not 
moved  at  all.  The  forward  current  is  most  rapid  in  front,  becoming 
slower  at  the  rear,  exactly  as  in  Amoeba.  At  the  posterior  end  the 
surface  rolls  upward ;  particles  on  the  surface  which  were  at  first  on 
the  bottom  may  be  seen  to  pass  upward  around  the  posterior  end  and 
then  forward,  as  in  Amoeba.  The  form  of  the  drop  may  become  much 
elongated ;  the  anterior  edge  is  thin,  the  posterior  end  thick  and 
rounded.     In  all  these  respects  the  drop  resembles  the  moving  Amoeba. 


no  TIfE    BEHAVIOR    OF    I.OWKB    ORGANISMS. 

By  inclining  the  vessel  the  drop  may  be  made  to  roll  away  from  the 
attractive  spot ;  then  when  the  level  is  restored  it  moves  back  again. 
By  repeating  this  process  the  movements  may  be  studied  in  detail. 
P*or  studying  the  movements  in  all  parts  except  at  the  anterior  edge 
another  more  convenient  method  may  be  employed.  A  small  piece  of 
wood  may  be  brought  against  one  side  of  the  drop ;  toward  this  it 
moves  in  the  manner  just  described.  If  the  piece  of  wood  is  moved 
continually  in  a  certain  direction,  the  drop  follows,  and  its  movements 
may  be  examined  with  ease.  In  this  case  the  anterior  edge,  of  course, 
is  not  thin  and  pressed  against  the  surface,  but  otherwise  the  move- 
ments are  the  same. 

By  proper  modifications  further  details  of  the  movement  of  Amccba 
are  exactly  imitated.  Thus  a  quantity  of  sand  grains  or  other  heavy 
objects  may  be  added  to  the  drop.  In  the  movement  these  collect  at 
the  posterior  end,  as  happens  with  the  coarse  internal  contents  in 
Amoeba.  A  large,  spherical  bubble  of  oil  may  be  introduced  into  the 
drop,  in  imitation  of  the  contractile  vacuole ;  this  likewise  stays  near 
the  posterior  end.  When  a  considerable  quantity  of  heavy  material  is 
collected  at  the  posterior  end,  the  latter  becomes  drawn  out  into  a  sort 
of  pouch,  which  is  dragged  along,  its  substance  not  partaking  of  the 
currents  shown  by  the  remainder  of  the  drop.  It  thus  plays  the  same 
part  as  the  well-known  posterior  appendage  of  Amoeba.  Material 
passes  up  from  the  bottom  to  the  upper  surface  on  each  side  of  this 
posterior  pouch,  just  as  happens  in  Amoeba  (see  p.  i6S).  Particles 
clinging  to  the  outer  surface  at  the  posterior  end  are  often  dragged 
along  for  a  considerable  time,  then  finally  pass  upward  to  the  upper 
surface  and  so  forward,  exactly  as  described  for  Amoeba  (p.  169).* 

In  another  detail  the  movements  of  the  drop  of  water  or  glycerine 
are  strikingly  like  those  of  Amoeba.  As  we  have  seen,  the  current  is 
most  rapid  at  the  anterior  end  in  both  cases,  becoming  as  a  rule  slow 
toward  the  rear.  But  I  have  pointed  out  that  in  Amoeba  the  move- 
ments at  the  posterior  end  are  not  uniform.  Sometimes  the  under  sur- 
face remains  attached  to  the  bottom  longer  than  usual,  then,  when  it 
becomes  detached  over  a  considerable  area  at  once,  there  is  a  sudden 
rush  of  the  fluid  forward  from  the  posterior  region  (p.  16S).  Exactly 
the  same  thing  is  to  be  observed  in  the  inorganic  drop.  The  bottom 
is  not  uniform,  so  that  sometimes  the  posterior  end  clings  to  it  longer 
than  usual ;  this  end  is  then  drawn  out,  and  when  it  is  finally  released 

*It  may  be  worth  while  to  state  that  these  experiments  on  inorganic  fluids 
were  performed  after  the  work  on  the  movements  of  Amoeba  had  been  completed 
and  the  description  entirely  written  in  the  form  given  in  the  preceding  pages. 
No  details  of  the  movements  of  Amoeba  were  added  after  the  behavior  of  the 
inorganic  drops  had  been  studied^ 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  211 

there  is  a  sudden  rush  forward  of  the  internal  fluid  from  this  region, 
giving  the  movement  a  jerky  character. 

Still  another  resemblance  in  detail  between  the  movements  of  the 
inorganic  drop  and  of  Amoeba  may  be  noted  at  times.  As  we  have 
seen,  in  the  posterior  part  of  Amoeba  that  is  detached  from  the  bottom 
there  is  a  movement  forward  not  only  on  the  upper  surface,  but  also  a 
slow  movement  on  the  lower  surface ;  the  entire  posterior  region  is 
contracting.  The  same  thing  may  be  seen  in  the  inorganic  drop.  The 
phenomenon  in  question  is  not  so  regular  here,  because  the  posterior 
half  usually  still  clings  to  the  surface  to  a  certain  extent,  while  in  Amoeba 
it  is  as  a  rule  entirely  free.  But  when  the  posterior  half  of  the  inor- 
ganic drop  does  become  entirely  free,  it  is  seen  to  contract  as  a  whole, 
with  a  forward  movement  on  both  upper  and  lower  surfaces,  exactly 
as  in  Amoeba. 

One  may  even  see  at  times,  under  special  conditions,  a  slight  turning 
backward  of  the  current  at  the  sides  of  the  anterior  end,  such  as  has 
been  described  by  a  number  of  authors  for  Amoeba  (see  p.  137).  This 
occurs  when  the  drop  is  slender  and  elongated,  and.  the  area  on  which 
it  spreads  out  is  broad.  On  coming  in  contact  with  the  area,  the  end 
of  the  drop  rushes  forward  and  spreads  out.  If  the  whole  width  of  the 
area  is  not  covered  at  first,  some  of  the  particles  that  have  moved  for- 
ward curve  outward  and  a  little  backward  till  the  area  is  quite  covered. 

Altogether,  the  resemblance  between  the  movements  of  the  inor- 
ganic drop  and  those  of  Amoeba  is  extraordinary,  extending  even  to 
details.  What  are  the  forces  at  work  in  such  a  drop,  and  in  how  far 
may  they  be  supposed  to  be  active  also  in  Amoeba.'* 

The  spreading  out  of  the  drop  of  glycerine  or  water  at  the  anterior 
end  is  due  to  its  adherence  here  to  the  substratum.  The  remainder  of 
the  movements  of  the  inorganic  drop  are  due  to  the  interplay  of  surface 
tension  and  adhesion  to  the  substratum.  As  a  result  of  surface  tension 
the  drop  seeks  to  regain  its  spherical  form  ;  hence  the  posterior  part  is 
pulled  forward,  the  force  required  to  accomplish  this  being  less  than 
would  be  demanded  for  freeing  the  anterior  edge  from  the  substratum. 
In  the  pulling  forward  of  the  posterior  portion  the  adherence  of  the 
lower  surface  to  the  bottom  keeps  this  surface  from  moving ;  hence  the 
upper  surface  moves  forward  while  the  lower  surface  remains  quiet 
or  moves  forward  only  very  slowly ;  the  movement  is  thus  converted 
into  a  rolling  motion.  The  details  given  above  depend  merely  upon 
the  relative  part  played  by  adherence  and  surface  tension,  with  the 
resistance  offered  by  the  weight  and  inertia  of  particles  inclosed  in  the 
drop. 

In  Amoeba,  so  far  as  the  evidence  of  observation  goes,  the  conditions 
are  similar.     Amoeba  adheres  to  the  substratum  and  spreads  out  in  a 


212  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

similar  manner.  In  one  respect  there  is,  of  course,  a  striking  differ- 
ence between  the  two  cases.  Amoeba  does  not  require  that  the  sub- 
stratum should  be  different  on  its  two  sides  in  order  that  there  should 
be  movement ;  on  the  contrary,  it  may  move  steadily  in  a  certain  direc- 
tion on  a  uniform  surface.  The  mechanism  of  the  movement  might, 
nevertheless,  be  the  same  as  in  the  inorganic  drop.  Chemically  different 
substances  show  different  degrees  of  adherence  to  the  same  surface.  It 
may  be  supposed,  therefore,  that  there  is  a  chemical  difference  between 
the  anterior  and  posterior  regions  of  Amoeba  of  such  a  nature  that  the 
anterior  region  clings  to  the  surface  while  the  posterior  region  does  not. 
This  chemical  difference  must,  of  course,  be  continually  renewed,  since 
new  parts  of  the  body  continually  come  in  contact  with  the  substratum. 

It  may,  however,  be  questioned  whether  the  adhesion  of  Amoeba  to 
the  substratum  is  of  the  same  character  as  the  adhesion  of  a  drop  of 
water  to  glass  ;  in  other  words,  whether  Amoeba  really  plays  here  the 
part  of  a  fluid,  and  "  wets"  the  substratum.  This  was  the  view  taken 
by  Berthold  (1886)  and,  if  I  understand  him  correctly,  Le  Dantec 
(1895).  Apparently  opposed  to  such  a  view  is  the  fact  that  Amoeba 
may  creep  on  the  under  side  of  the  surface  film  of  water,  as  I  have 
often  observed.  This  surface  film  is,  of  course,  fluid  ;  if  in  adhesion 
Amoeba  itself  also  plays  the  part  of  a  fluid,  we  should  have  two  fluids 
in  contact,  having  the  same  relation  of  attraction  or  adhesion  that  a 
fluid  has  for  a  solid  that  it  "  wets"  ;  that  is,  the  particles  of  each  fluid 
have  a  greater  attraction  for  those  of  the  other  fluid  than  for  each  other. 
This,  it  would  appear,  could  result  only  in  the  formation  of  diffusion 
currents  in  the  two  fluids  ;  the  two  would  mix.  This  result  does  not 
follow,  so  that  it  would  appear  that  in  adhesion  Amoeba  does  not  play 
simply  the  part  of  a  fluid  which  wets  the  substratum.  As  we  have 
seen  (p.  165),  there  is  evidence  that  the  adhesion  takes  place  through 
the  mediation  of  a  viscid  secretion. 

Whatever  the  nature  of  the  adhesion,  we  know  it  exists  at  one  pole 
of  the  Amoeba  and  not  at  the  other.  Given  such  chemical  difl!erences 
between  the  two  poles  as  would  produce  this  difference  in  adhesion, 
then  locomotion  would  follow  essentially  as  we  find  it  to  occur  in 
Amoeba  Umax  or  A.  verrucosa.  No  further  properties  except  those 
common  to  fluids  would  be  required.*  For  the  determination  of  the 
direction  and  rate  of  locomotion,  the  distribution  of  these  chemical 
diflJerences  would  be  the  essential  factor. 

Caution  is  necessary,  however,  in  transferring  the  results  of  these  and 
other  similar  experiments  to  Amoeba.  The  resemblances  between  the 
movements  of  the  inorganic  drops  and  those  of  Amoeba  show  merely 

*It  will  be  noted  that  this  statement  is  made  for  simple  locomotion,  and  does 
not  refer  to  the  formation  of  pseudopodia. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  213 

that  the  forces  acting  upon  the  two  have  a  similar  localization  and 
direction,  not  necessarily  that  the  forces  themselves  are  identical.  This 
caution  is  emphasized  by  the  fact  that  drops  moving  down  an  inclined 
plane  as  a  result  of  the  action  of  gravity  have  a  similar  rolling  motion. 
This  is  well  shown  in  the  drops  of  glycerine  or  water  on  the  oiled 
surface,  in  the  experiments  just  described.  Most  (though  not  all)  of 
the  details  mentioned  above,  in  which  the  movements  of  the  inorganic 
drop  resemble  those  of  Amoeba,  may  be  observed  also  in  drops  moving 
under  the  influence  of  gravity.  The  essential  difference  between  the 
two  sets  of  experiments  is  that  the  action  of  adhesion,  pulling  the  drop 
in  a  certain  direction  in  the  one  case,  is  replaced  by  the  action  of 
gravity,  pulling  in  the  same  direction,  in  the  other  case.  Correspond- 
ing with  this  difference  is  the  chief  difference  to  be  observed  in  the 
movements  of  the  drops  under  the  different  conditions.  In  those  mov- 
ing as  a  result  of  greater  adhesion  on  one  side,  the  anterior  edge  is 
thin  and  flat,  as  in  Amceba,  while  in  those  moving  from  the  action  of 
gravity  this  is  not  true. 

In  Amoeba  observation  shows  that  we  have  the  one-sided  greater 
adhesion,  and  the  tendency  of  the  lower  surface  to  cling  slightly  to  the 
substratum,  as  in  the  first  set  of  experiments  with  the  inorganic  drops. 
There  remains  only  something  corresponding  to  the  surface  tension 
factor,  common  to  both  sets  of  inorganic  experiments,  to  be  accounted 
for  in  Amoeba.  Since  Amoeba  acts  like  a  fluid  in  many  respects,  there 
is  no  a  priori  reason  to  deny  it  surface  tension,  and  nothing  further  is 
required  to  produce  locomotion.  To  this  there  is,  however,  one  objec- 
tion. This  is  found  in  the  roughening  and  wrinkling  of  the  surface 
at  the  posterior  end  as  it  contracts,  and  in  the  similar  roughening  of  a 
contracting  pseudopodium  (pp.  i6o,  i68) .  This  is  exactly  the  opposite 
of  what  should  take  place  in  a  fluid  contracting  as  a  result  of  surface  ten- 
sion. In  such  a  case  the  primary  phenomenon  is  the  decrease  in  sur- 
face ;  the  latter  should,  therefore,  remain  perfectly  smooth,  and  as  small 
as  possible.  Of  course,  surface  tension  might  be  replaced  in  Amoeba 
by  a  specific  property  of  contractility  of  some  sort,  having  its  seat  a 
little  beneath  the  surface.  Locomotion  would  then  take  place  as  in 
the  inorganic  drop,  and  the  wrinkling  of  the  outer  surface  would  be 
accounted  for.  On  the  other  hand,  if  we  can  account  for  the  contrac- 
tility by  a  known  property  of  fluids,  such  as  surface  tension,  our  expla- 
nation will,  of  course,  be  simpler  and  more  probable.  By  taking  into 
consideration  the  apparent  fact  that  the  outer  layer  of  Amoeba  is  partly 
fluid,  partly  solid,  I  believe  that  such  an  explanation,  accounting  for 
the  roughening  as  well  as  the  contractility,  can  be  given  ;  this  I  shall 
attempt  in  the  next  section  of  this  paper  (p.  215). 

The  formation  of  projections  at  the  anterior  edge  or  side  of  the  inor- 
ganic drop,  comparable  to  the  formation  of  pseudopodia  in  contact  with 


214  '^"^    BEHAVIOR    OF    LOWER    ORGANISMS. 

the  substratum  in  Amoeba,  may  also  be  induced  in  the  oil  drops.  For 
this  purpose  it  is  necessary  to  produce  a  greater  adhesion  on  a  small 
area  at  one  side.  A  projection  is  at  once  sent  out  here.  The  move- 
ment in  sending  out  such  a  projection  is  the  same  as  that  to  be  observed 
in  the  formation  of  a  pseudopodium  under  such  circumstances.  The 
projection  is  thinnest  at  the  tip  ;  its  upper  surface  moves  forv^'ard  and 
rolls  over  at  the  point,  while  the  lower  surface  is  at  rest. 

FORMATION   OF   FREE    PSKUDOPODIA. 

On  the  other  hand,  the  projection  of  free  pseudopodia  into  the  water 
cannot  be  imitated  under  these  conditions.  As  we  have  seen,  the  move- 
ment in  the  formation  of  a  free  pseudopodium  differs  from  that  in  form- 
ing a  pseudopodium  along  a  surface  merely  in  the  fact  that  in  the  latter 
case  the  contact  surface  is  at  rest,  while  in  the  free  pseudopodium  all 
surfaces  move  equally,  a  given  point  on  the  surface  remaining  approx- 
imately at  the  same  distance  from  the  tip.  In  the  inorganic  drop  pro- 
jections can  indeed  be  formed  in  which  the  surface  moves  in  exactly 
the  same  manner  as  in  the  free  pseudopodia  of  Amoeba,  but  under  con- 
ditions that  are  essentially  different.  If  some  small  object  to  which  the 
fluid  adheres,  such  as  a  sliver  of  wood,  is  brought  into  contact  with  one 
side  of  the  drop,  the  fluid  flows  out  over  it,  and  may  form  thus  a  long, 
slender  projection.  The  surface  of  this  projection  moves  in  the  same 
manner  as  the  surface  of  a  pseudopodium  in  Amoeba  (p.  153).  Thus 
the  surface  of  a  free  pseudopodium  shows  such  movements  as  it  would 
if  drawn  out  by  an  object  to  which  it  adheres  at  its  tip.  Since  no  such 
object  is  present,  it  is  clear  that  the  formation  of  free  pseudopodia  is  not 
explicable  in  this  manner. 

As  we  have  seen  above,  the  locomotion  and  the  formation  of  pseudo- 
podia in  contact  with  the  substratum  could,  if  they  stood  alone,  be  con- 
sidered due  to  the  adherence  and  spreading  out  of  a  fluid  on  a  solid,  as 
maintained  by  Berthold  (18S6).  But  they  do  not  stand  alone  ;  we  have 
the  additional  fact  that  pseudopodia  may  be  sent  out  which  are  not  in 
contact  with  the  substratum .  The  anterior  edge  of  an  Amoeba,  further, 
may  be  pushed  out  freely  into  the  water  as  a  single  pseudopodium. 
This  may  frequently  be  seen  in  Amoeba  Umax.  As  a  reaction  to  a 
.stimulus  the  protoplasm  may  push  upward  freely  as  a  thick  lobe,  till 
the  greater  part  of  the  substance  is  transferred  upward  and  the  Amoeba 
topples  over  (p.  184) .  In  the  formation  of  such  a  lobe,  the  protoplasm 
may  flow  from  both  ends  toward  the  middle,  producing  the  '*  heaping 
up"  from  which  the  thick  upward  projection  results  (see  p.  183). 
Currents  flowing  in  this  manner  could  not  possibly  be  produced  by 
adherence  to  the  substratum.  Again,  in  an  advancing  Afiioeba  avgu- 
lata^  short  triangular  pseudopodia  are  constantly  pushed  forward,  some 
in  contact  with  the  substratum,  others  not  thus  in  contact,  but  raised  a 


THE    MOVEMKVTS    AND    REACTIONS    OF    AMCEBA.  21^ 

little  above  it  (Fig.  54).  Some,  which  are  at  first  free,  later  come  in 
contact.  Clearly,  Amoeba  is  able  to  perform  all  the  activities  con- 
cerned in  locomotion  without  adherence  to  a  solid.  The  adherence 
is  only  necessary  that  there  may  be  a  movement  from  place  to  place. 
The  case  is  quite  parallel  to  that  of  higher  organisms,  where  contact 
with  the  substratum  is  necessary  in  order  that  progression  may  occur, 
though  all  the  movements  concerned  in  locomotion  may  be  performed 
without  such  contact. 

We  are  compelled  to  conclude,  therefore,  that  in  the  advancing  end  of 
an  Amoeba  or  the  projecting  pseudopodium  there  is  an  active  move- 
ment of  the  protoplasm,  of  a  sort  which  has  not  been  physically 
explained.  This  involves  the  general  conclusion  that  no  physical 
explanation  is  at  present  possible  of  the  locomotion  and  projection  of 
pseudopodia  in  Amoeba. 

To  account  for  the  contraction  of  the  posterior  part  of  the  body,  on 
the  other  hand,  possibly  the  properties  common  to  Amoeba  with  other 
fluids  are  sufficient.  If  surface  tension  may  be  considered  the  cause  of 
the  contraction  of  the  posterior  part  of  the  body,  it  is  notable  that  it 
acts  as  a  constant  factor,  tending  always  to  decrease  the  surface  as  much 
as  postiible,  not  as  a  variable  factor.  In  other  words,  there  is  no  indi- 
cation that  local  increase  or  decrease  in  surface  tension  (see  note,  p. 
235)  plays  any  part  in  the  production  of  the  movements,  as  is  main- 
tained in  the  prevailing  theories.  The  part  played  by  surface  tension 
is  thus  a  very  subordinate  one. 

EXPERIMENTAL  IMITATION  OF  MOVEMENTS  DUE  TO  LOCAL  CON- 
TRACTIONS OF  THE  ECTOSARC,  AND  OF  THE  ROUGHENING  OF 
THE    ECTOSARC    IN    CONTRACTION. 

Besides  the  sending  out  of  pseudopodia,  there  are  certain  other  phe- 
nomena in  the  movements  of  Amceba  for  which  we  lack,  so  far  as  I  am 
aware,  any  attempt  at  a  physical  explanation.  These  are  the  swinging 
movements,  vibrations,  and  local  contractions  of  pseudopodia,  described 
on  pages  1 77-1 79,  and  the  roughening  of  the  ectosarc  in  the  contraction 
of  pseudopodia  or  other  parts  of  the  body  (p.  16S). 

These  phenomena  are  in  certain  details  so  similar  to  some  that  I 
have  observed  in  inorganic  fluids  that  I  believe  it  worth  while  to 
analyze  the  latter ;  possibly  they  give  an  indication  of  the  direction  in 
which  an  explanation  of  the  phenomena  in  Amoeba  above  mentioned 
nay  lie.* 

♦In  view  of  the  repeated  failures  of  physical  explanations  in  attempting  to 
account  for  vital  phenomena,  one  does  not  approach  a  new  attempt  of  this  sort 
with  great  confidence.  Yet  it  is  desirable  that  any  possibility  of  this  kind  should 
be  worked  out  and  submitted  to  criticism,  in  order  that  its  truth  or  lack  of  truth 
mav  be  demonstrated. 


2l6  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

Swinging  or  bending  movements  take  place  with  special  frequency 
while  the  pseudopodia  are  withdrawing ;  in  some  Amoebae  such  move- 
ments are  an  almost  constant  accompaniment  of  withdrawal.  As  it  is 
withdrawn  the  pseudopodium  becomes  roughened  or  warty  on  its  sur- 
face, as  we  have  seen,  and  at  the  same  time  bends  to  one  side  or  the 
other,  or  swings  back  and  forth.  The  impression  given  is  that  the 
outer  layer  of  the  pseudopodium  has  become  partially  solid.  In  with- 
drawing, the  solid  substance  seems  to  melt  gradually  away,  in  a  some- 
what irregular  manner,  so  as  to  leave  solid  masses  connected  by  liquid 
protoplasm,  the  projecting  solid  masses  forming  the  wart-like  roughen- 
ings  of  the  surface.  When  this  melting  away  occurs  more  strongly  on 
one  side,  the  pseudopodium  bends  at  that  point,  toward  the  side  which 
has  apparently  become  more  fluid. 

We  have  in  such  a  case,  if  appearances  may  be  trusted,  a  mass  com- 
posed partly  of  solid,  partly  of  fluid.  While  it  is  usually  admitted  that 
parts  of  the  protoplasm  may  become  solid  at  times,  little  attempt  has 
been  made  to  understand  protoplasmic  movements  by  studying  the 
physics  of  such  mixtures  of  solids  and  fluids.*  In  certain  experiments 
with  inorganic  mixtures  of  this  kind,  in  which  movements  were  pro- 
duced that  resembled  those  just  referred  to  in  Amoeba,  the  writer 
became  convinced  of  the  possible  importance  of  the  physics  of  such 
mixtures  for  the  understanding  of  protoplasmic  activities. 

The  experiments  in  question  were  concerned  with  the  movements 
under  the  action  of  surface  tension  of  oil  drops  to  which  soot  had  been 
added  for  the  purpose  of  rendering  the  currents  visible.  When  a  large 
quantity  of  soot  was  added,  the  drops  became  somewhat  stiffened,  and 
now  showed  to  a  marked  degree  a  mingling  of  the  characteristic  proper- 
ties of  fluids  and  solids. 

In  one  set  of  experiments  clove  oil  was  thus  mixed  with  soot  and 
introduced  as  drops  into  a  mixture  of  three  parts  glycerine  and  one  part 
95  per  cent  alcohol.  The  drops  move  about,  as  a  result  of  local 
decrease  in  surface  tension,  in  the  same  manner  as  the  olive-oil  emul- 
sion in  Biitschli's  celebrated  experiments.  Much  of  the  soot  collects 
next  to  the  surface  of  the  drop,  and  becomes  massed  in  certain  regions, 
as  a  result  of  the  currents,  covering  these  regions  with  a  sort  of  crust, 
this  crust  being  formed  of  separate  solid  particles.  The  particles  are 
crowded  together  as  closely  as  possible,  owing  to  the  surface  tension  of 
the  fluid  in  which  they  are  floating-t  If  the  particles  are  not  too  minute 
they  may  project  above  the  surface  of  the  drop,  giving  it  a  rough  appear- 

♦Some  of  the  experiments  of  Rhumbler  (1898,  1902)  deal  with  such  mixtures, 
though  not  with  a  view  to  an  understanding  of  the  movements,  but  of  certain 
other  processes. 

t  According  to  the  principles  set  forth  by  Rhumbler,  1898,  p.  332. 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  21 7 

ance,  similar  to  that  of  the  withdrawing  pseudopodium  of  Amoeba. 
Such  parts  of  drops  or  whole  drops,  so  covered,  show  peculiar  proper- 
ties. The  form  may  be  changed  by  lowering  the  surface  tension  locally 
or  by  mechanical  action  from  outside,  exactly  as  in  a  fluid,  but  there 
is  an  inclination  to  hold  a  form  once  received.  The  tendency  to  take 
the  spherical  form  is  still  somewhat  marked,  and  if  the  irregular  drop 
is  strongly  disturbed  it  frequently  slowly  becomes  spherical.  On  the 
other  hand,  if  not  strongly  disturbed,, it  may  retain  almost  any  form 
impressed  upon  it — cylindrical,  flattened,  irregular,  or  with  long,  slender 
projections.  In  this  power  of  receiving  and  retaining  an  irregular  form, 
yet  with  a  tendency  to  become  spherical,  these  drops,  of  course,  resem- 
ble Amoeba.  These  properties  vary  with  the  amount  of  soot  present  in 
the  oil ;  if  this  is  less,  the  drops  slowly  return  to  the  spherical  shape 
when  deformed  ;  if  greater,  they  retain  the  irregular  shape  indefinitely. 
Such  irregular  masses  nevertheless  flow  together  if  brought  in  contact, 
will  quickly  gather  together  into  a  close  mass  if  strongly  deformed, 
and  in  many  other  ways  they  show  the  characteristics  of  fluids. 

The  reason  for  their  tendency  to  retain  irregular  forms  is  obvious. 
The  surface  is  covered  with  small  solid  particles  that  are  in  contact. 
The  projection  of  these  particles  above  the  surface  may  cause  a  rough- 
ening of  the  surface.  Any  change  of  form,  such  as  surface  tension 
would  produce,  causes  much  friction  between  these  particles.  The 
form  taken  is,  then,  a  resultant  of  the  action  of  surface  tension  and  the 
resistance  of  these  particles  to  movements.*  Similar  forms  are  pro- 
ducible by  mixing  soot  with  bone  oil  and  studying  drops  of  the  mixture 
in  a  vessel  of  glycerine. 

For  our  purpose  the  phenomena  which  occur  when  the  soot  particles 
are  unequally  distributed  are  of  special  interest.  Consider  an  elon- 
gated projection,  as  in  Fig.  7S,  A,  with  the  surface  entirely  covered 
with  closely  crowded  soot  particles  except  in  a  certain  region,  x-y,  on 
one  side.  In  this  region  x-y  surface  tension  will  have  free  play,  tend- 
ing to  draw  the  points  x  and  y  together,  while  elsewhere  the  tendency 
to  contraction  will  be  resisted  by  the  friction  of  the  particles.  The 
result  is  that  the  points  x-y  are  drawn  together,  and  the  projection 
bends  toward  that  side.  Since  this  bending  does  not  tend  to  crowd 
the  particles  on  other  parts  of  the  surface  closer  together  they  do  not 
resist  it. 

In  the  oil  drops  mixed  with  soot  the  bending  of  projections  in  the 
manner  described  is  often  to  be  observed  under  the  appropriate  condi- 
tions.    They  should  be  compared  with  the  bending  of  pseudopodia  as 


*  Similar  forms  of  fluids  have  been  produced  by  Rhumbler  in  a  parallel  man- 
ner in  his  imitations  of  the  formation  of  Difllugia  shells  (1898,  p.  287)  and  of 
the  shapes  of  the  shells  of  Foraminifera  (1902,  p.  265). 


2l8  THK    BKHAVIOR    OF    LOWER    ORGANISMS. 

described  for  Amoeba  (p.  177,  and  Fig.  62,  a) .  The  chief  experimental 
difficulty  in  producing  such  bending  is  to  arrange  the  conditions  in 
such  a  way  that  there  is  less  soot  on  one  side  of  a  projection  than  on 
the  other.  This  occurs  somewhat  frequently  when  two  irregular  drops 
are  allowed  to  fuse,  or  when  a  drop  is  mechanically  deformed  with  a 
rod,  as  described  in  the  next  paragraph.  One  can  sometimes  bring  it 
about  by  placing  with  the  capillary  pipette  a  minute  drop  of  oil  on  one 
side  of  a  projection,  though  this  method  is  not  as  a  rule  very  effective. 
*^,  -  Such  drops  may  also  show  another  prop- 

,  erty  in  common  with    Amoeba,   namely, 
elasticity  of  form,  or  a  phenomenon  pro- 
ducing similar  results.     Consider  a  curved 
projection,  as  in  Fig.  78,  B.     It  is  com- 
P       ^^^  pletely  covered  with  soot  particles  and  re- 

tains its  form  in  virtue  of  their  resistance  to  a 
change  in  position.  Now,  suppose  we  forcibly  straighten  out  the  pro- 
section  by  pushing  it  to  one  side  with  a  rod.  By  so  doing  the  side  a-6 
is  lengthened  ;  the  soot  particles  on  this  side  are,  therefore,  separated, 
leaving  certain  areas  of  free  fluid  surface.  When  the  projection  is 
released,  surface  tension  can  act  on  these  areas,  and  the  projection  is 
drawn  back  at  once  to  its  original  form.  I  have  often  observed  such 
immediate  returns  to  the  original  form  after  bending  a  projection  of 
one  of  the  oil  drops. 

In  Amoeba  we  have  exactly  the  conditions  most  favorable  for  the 
production  of  movements  of  this  sort,  and  we  actually  find  numerous 
movements  of  just  this  character.  It  is  generally  admitted  that  the 
outer  layer  becomes  partially  solidified  ;  as  a  pseudopodium  is  with- 
drawn the  solid  portions  evidently  become  liquefied  in  an  irregular 
way,  some  of  them  projecting  above  the  surface  and  making  it  rough. 
If  the  liquid  substance  produced  shows  surface  tension,  the  movements 
described  must  follow  in  the  manner  set  forth  above.  It  seems  possible 
that  many  of  the  observed  movements  are  thus  produced  by  local  lique- 
faction, with  the  intervention  of  surface  tension,  in  the  liquefied  area. 
In  view  of  the  apparently  unlimited  possibilities  of  partial  solidifica- 
tion and  liquefaction  in  the  protoplasmic  body,  with  the  resulting  varied 
action  of  surface  tension,  shall  we  not  go  a  step  farther  and  inquire 
whether  there  may  not  be  an  outlook  for  an  explanation  of  vibratory 
movements,  such  as  we  find  in  flagella,  along  this  line.?  In  an  elon- 
gated structure  like  a  flagellum,  a  limited  liquefaction  of  one  side  would 
result  in  a  bending  toward  this  side.  By  regular  alternation  of  lique- 
factions in  different  regions,  a  regular  vibration  could  be  produced. 
Th^  chief  difficulty  in  the  way  of  such  a  theory  would  seem  to  lie  in 

*FiG,  78. — Diagrams  illustrating  phenomena  in  mixtures  of  oil  and  soot. 


THE    MOVEXfENTS    AND    REACTIONS    OF    AMCEBA.  2lC) 

the  restoration  of  the  original  length  in  a  given  side  after  liquefaction 
and  consequent  contraction  had  occurred.  This  could,  perhaps,  be 
brought  about  by  an  elastic  rod  in  the  axis  of  the  structure,  such  as 
many  cilia  and  flagella  are  known  to  possess. 

The  above  is  merely  a  suggestion  made  tentatively  ;  its  justification 
as  a  suggestion  lies  in  the  following  facts:  (i)  The  swinging  move- 
ment of  pseudopodia  in  Amoeba  in  some  cases  strikingly  resembles 
movements  of  the  character  above  set  forth  in  inorganic  fluids,  and 
precisely  the  conditions  for  such  movements  are  present  in  Amoeba  ; 
(2)  Swinging  movements  of  pseudopodia  seem  to  grade  almost  insen- 
sibly into  the  vibratory  movements  of  flagella. 

DIRECT     OR     INDIRECT     ACTION     OF     EXTERNAL     AGENTS     IN 
MODIFYING    THE    MOVEMENTS. 

Is  the  efl*ect  of  external  agents  in  modifying  the  movements  of  Amoeba 
due  to  the  direct  physical  action  of  the  agent  on  that  part  of  the  fluid 
substance  with  which  it  comes  in  contact?  Or  is  its  action  indirect, 
in  that  it  serves  merely  as  a  stimulus  to  certain  internal  changes,  the 
latter  bringing  about  the  modifications  in  the  behavior?  Both  views 
find  adherents.  The  difference  between  them  is  fundamental,  for  they 
lead  to  essentially  different  conceptions  as  to  the  nature  of  behavior  in 
these  lower  organisms. 

In  higher  animals  we  know  that  the  movements  and  changes  of 
movement  are  not  produced  in  a  direct  way,  but  the  effect  of  external 
agents  is  to  cause  internal  alterations  which  result  in  changes  of  move- 
ment. It  is  not,  therefore,  possible  to  predict  the  movements  of  the 
organism  from  a  knowledge  of  the  direct  physical  changes  produced  in 
its  substance  by  the  agent  in  question.  If  the  theory  of  direct  action  is 
correct  for  Amoeba,  we  have  in  these  animals  a  condition  of  affairs  incom- 
parably simpler,  for  here  we  can  resolve  the  behavior  directly  into  its 
physical  factors.  If,  on  the  other  hand,  the  theory  of  indirect  action  is 
correct,  then  there  appears  to  be  nothing  fundamentally  different  in 
principle  between  the  behavior  of  Amoeba  and  that  of  higher  organisms. 

How  the  form  and  movement  of  a  fluid  mass  might  be  determined 
by  the  direct  action  of  external  agents  on  its  surface  may  be  simply 
illustrated  by  certain  experiments  which  I  have  described  elsewhere 
(Jennings,  1902).  A  mixture  of  2  parts  glycerine  and  i  part  95  per 
cent  alcohol  is  placed  on  a  slide  and  covered  with  a  cover  glass  sup- 
ported by  glass  rods.  Into  this  is  introduced  with  a  capillary  pipette 
a  drop  of  clove  oil.  The  clove-oil  drop,  at  first  circular  in  form,  soon 
changes  shape,  shows  internal  currents,  sends  out  projections  in  various 
directions,  moves  about  from  place  to  place,  and  may  divide  into  two 
drops.  The  alcohol,  not  being  uniformly  distributed  throughout  the 
glycerine,  acts  more  strongly  on  some  parts  of  the  clove-oil  drop  than 


220  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

on  others,  thus  lowering  the  surface  tension  in  the  region  acted  upon. 
Thereupon  the  drop  sends  out  a  projection  on  the  side  affected,  and  may 
follow  this  up  by  moving  in  that  direction.  We  may  cause  the  drop  to 
send  out  projections  and  move  in  a  certain  direction  by  placing  a 
minute  drop  of  alcohol  near  one  side,  or  by  heating  one  side ;  move- 
ment takes  place  toward  the  side  affected.  These  agents  act  directly 
on  the  surface  of  the  drop,  lowering  the  tension  ;  the  movements  are  a 
direct  consequence  of  this  change.  Parallel  phenomena  may  be  pro- 
duced, as  Bernstein  (1900)  has  shown,  with  a  drop  of  quicksilver.  If 
such  a  drop  is  placed  in  10  per  cent  nitric  acid,  in  which  bichromate 
of  potash  has  been  dissolved,  the  drop  changes  form  and  moves  about. 
If  we  place  near  such  a  drop,  in  vessel  of  10  per  cent  nitric  acid,  a 
crystal  of  potassium  bichromate,  the  mercury  drop  moves  rapidly  over 
to  the  crystal.  Here,  again,  the  chemical  acts  directly  on  the  mercury, 
lowering  the  surface  tension  at  the  region  where  it  comes  in  contact 
with  it,  thus  producing  the  movement. 

Certain  authors  have  held  that  the  movements  of  Amoeba  are  pro- 
duced in  this  way  by  the  direct  action  of  external  agents  decreasing 
or  mcreasing  the  surface  tension  of  certain  parts  of  the  fluid  mass.  As 
an  example  of  the  theory  of  direct  action  of  external  agents  in  control- 
ling the  behavior,  we  may  take  the  view  of  the  reaction  of  Amoeba  to 
chemicals  recently  given  by  Rhumbler  (1902,  p.  384).  According  to 
Rhumbler,  it  is  evident  that  when  an  Amoeba  moves  toward  or  away 
from  a  certain  chemical,  the  side  directed  toward  the  chemical  has,  in 
the  first  case,  a  lessened  surface  tension,  in  the  second  case  an  increased 
surface  tension,  as  compared  with  the  remainder  of  the  body. 

The  necessary  differences  of  tension  on  the  positive  and  negative  sides  may  be 
easily  understood  from  our  present  standpoint,  by  holding  that  a  positively 
acting  chemical  decreases  the  surface  tension  both  in  the  living  alveolar  system 
of  the  cell  and  especially  on  the  cell  surface,  upon  which  it  must  work  most 
strongly;  that  a  negatively  acting  chemical,  on  the  other  hand,  produces  an 
increase  of  surface  tension  in  the  alveoli  of  the  cell,  and  especially,  again,  on  the 
cell  surface;  this  increase  is  the  greater,  and  from  a  physical  standpoint  must  be 
the  greater,  the  more  the  molecules  of  the  chemical  affect  or  modify  the  tension 
of  the  different  cell  alveoli  or  different  parts  of  the  cell  surface  (/.  c,  p.  384). 

The  explanation  of  thermotaxis  and  electrotaxis  would  be,  according 
to  Rhumbler,  ''exactly  the  same  as  for  chemotaxis"  (/.  c,  p.  385)  ; 
thus  also  as  a  result  of  the  direct  action  of  external  agents.  A  fuller 
explanation  of  the  "  tropisms  "  on  this  basis  is  given  by  Rhumbler  in 
an  earlier  paper  (1898,  pp.  183,  188).* 

♦  Rhumbler  emphasizes  in  the  paper  just  cited  (1898,  p.  184)  the  importance 
of  *' inner  disposition  "  in  deciding  what  effect  shall  be  produced  by  external 
agents,  but  in  the  tropisms,  at  least,  he  considers  the  action  of  the  external  agent 
to  be  direct,  the  inner  disposition  deciding  merely  whether  the  substance  of  the 
Amoeba  is  of  such  a  character  as  to  admit  of  the  production  of  a  given  definite 
change  in  surface  tension  by  the  outer  agent. 


THE    MOVEMEr^TS   AND    REACTIONS    OF   AMCEBA.  221 

Based  similarly  on  a  direct  action  of  external  agents  is  the  theory  of 
amoeboid  movements  proposed  by  Verworn  in  1891,  and  extended  in 
his  paper  on  Die  Bewegung  der  lebendtgen  Substanz  (1892)  and  in 
the  Allgemeinc  Physiologie,  In  its  original  form  Verworn^s  theory 
considers  the  movements  and  changes  of  form  to  be  brought  about 
directly  through  chemical  attraction  (Verworn,  1891,  p.  105),  but  in 
later  publications  (1892,  1895)  the  effect  of  the  chemical  is  considered, 
as  in  Rhumbler's  theory,  to  be  that  of  increasing  or  decreasing  the 
surface  tension. 

Thus  it  is  evident  that  it  must  be  the  chemical  affinity  of  certain  parts  of  the 
protoplasm  for  oxygen  that  decreases  the  surface  tension  in  definite  regions  and 
thus  leads  to  the  formation  of  pseudopodia.  But  it  will  be  possible  for  the  same 
effect  to  be  produced  by  other  substances  of  the  surrounding  medium,  if  they 
have  chemical  affinity  for  certain  components  of  ihe  protoplasm.  In  the  case 
where  the  substance  acts  from  one  side,  this  principle  must  lead  to  positive 
chemotropism.     (Verworn,  1895,  p.  545.) 

It  is  evident  that  the  method  of  movement  of  Amoeba,  as  described 
in  this  paper,  has  an  immediate  bearing  on  the  question  of  direct  or 
indirect  action  of  external  agents.  If  the  action  of  an  external  agent 
is  to  increase  or  decrease  directly  the  surface  tension,  as  set  forth  by 
Rhumbler  and  Verw^orn,  this  effect  must  be  shown  in  the  characteris- 
tic currents  which  appear  in  any  fluid  when  the  surface  tension  is  thus 
locally  changed.  In  the  case  of  negative  chemotaxis  we  should  have 
an  axial  current  away  from  the  side  affected,  with  surface  currents 
toward  the  chemical,  as  indicated  in  the  figure  given  by  Rhumbler 
(1898,  p.  188).  In  positive  chemotaxis  both  sets  of  currents  should  be 
the  reverse  of  that  just  indicated. 

In  the  account  of  the  movements  set  forth  by  Biitschli  and  Rhumbler, 
the  currents  agreed  with  the  scheme  for  direct  action  above  set  forth. 
But  this  account  of  the  movements  was  erroneous,  as  we  have  seen. 
The  internal  currents  and  the  surface  currents  are  forward,  away  from 
the  region  stimulated,  in  a  negative  reaction  ;  toward  the  region  stim- 
ulated in  a  positive  reaction ;  the  movement  is  of  a  rolling  character. 
There  is  thus  no  evidence  that  the  action  of  the  stimulus  is  to  cause  a 
change  in  the  surface  tension  of  the  parts  directly  affected  ;  on  the  con- 
trary, the  direction  of  the  currents  is  quite  inconsistent  with  this  view.* 
We  must  conclude,  then,  that  the  theory  of  the  direct  action  of  exter- 
nal agents  in  causing  or  changing  the  movements  of  Amoeba  is  nega- 
tived by  the  character  of  the  movements  produced  ;  these  are  not  such  as 
would  follow  from  the  direct  physical  action  of  the  agents  in  question. 

*  A  description  of  the  forward  surface  currents  in  negative  chemotaxis  is  given 
on  p.  143;  in  the  reaction  to  a  mechanical  stimulus  on  p.  185;  to  the  electrical 
stimulus  on  p.  192 ;  in  a  positive  food  reaction  (chemical  and  mechanical  stimuli  ?) 
on  p.  198. 


223  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

There  is  much  indirect  evidence  that  points  in  the  same  direction, 
particularly  in  the  fact  that  the  activities  of  the  animal  may  remain  con- 
stant while  the  environment  is  continually  changing.  Some  of  these 
lines  of  evidence  are  summarized  by  Rhumbler  (1898,  p.  185).  They 
still  leave  open  the  possibility  that  when  the  environment  does  modify 
the  movements  its  action  is  direct.  But  even  this  is  shown  to  be 
excluded  by  the  nature  of  the  currents  produced,  as  described  above. 

The  currents  as  they  actually  occur  in  the  movements  are  equally 
opposed  to  certain  theories  of  the  indirect  action  of  stimuli.  Bernstein 
(1900),  Jensen  (1901),  and  others,  have  expressed  the  opinion  that  the 
effect  of  stimuli  is  to  change  the  surface  tension,  but  that  this  eflect  is 
not  due  to  the  direct  physical  action  of  the  agent  on  the  protoplasm, 
but  rather  to  some  change  in  the  internal  physiological  processes  of  the 
cell  produced  by  the  agent  acting  as  a  stimulus.  Jensen  (1901,  1902) 
has  developed  this  view  into  a  detailed  theory,  according  to  which 
stimuli  that  increase  the  normal  assimilatory  processes  of  the  cell  lead 
to  a  reduction  of  surface  tension,  and  hence  to  expansion  and  move- 
ment toward  the  agent  in  question,  while  stimuli  that  increase  the 
dissimilatory  processes  have  the  opposite  effect. 

The  currents  in  the  moving  Amceba  lend  no  support  to  this  view. 
There  is  no  evidence  in  the  movement  that  the  efi'ect  of  a  stimulus  is  to 
alter  the  surface  tension  in  any  way.  In  view  of  the  facts  given  in  the 
body  of  this  paper  as  to  the  nature  of  the  movements,  we  are  forced  to 
give  up  the  idea  that  the  efiect  of  stimuli  is  to  modify  the  tension*  of 
the  surface  of  the  protoplasmic  mass,  either  directly  or  indirectly. 
Alterations  in  the  tension  of  the  surface  can  no  longer  be  considered 
the  prime  factor  in  the  behavior  of  Amceba. 

DIRECT    OR    INDIRECT    ACTION    IN    THE    TAKING    OF    FOOD. 

Rhumbler,  in  his  most  interesting  and  suggestive  paper  (1S9S),  has 
attempted  to  give  a  physical  analysis  of  food-taking  and  the  choice  of 
food  in  Amceba.  According  to  Rhumbler,  the  taking  of  food  is  due 
to  adhesion  between  the  protoplasm  and  the  food  substance,  and  may 
be  compared  with  the  pulling  inward  of  a  splinter  of  wood  by  a  drop  of 
water,  or  of  a  bit  of  shellac  by  a  drop  of  chloroform.  The  selection  of 
food  is  explained  as  due  to  the  fact  that  the  protoplasm,  as  might  be 
expected  from  physical  considerations,  tends  to  adhere  to  some  sub- 
stances and  not  to  others.  Parallel  phenomena  are  shown,  in  a  most 
ingenious  experiment,  to  be  demonstrable  for  the  chloroform  drop 
(/.  c,  p.  248).  It  takes  in  certain  substances,  while  others  are  refused 
or  thrown  out  if  introduced. 


♦See  note,  p.  225. 


THE    iMOVEMENTS    AND    REACTIONS    OF    AMCEBA.  223 

This  theory  is  a  most  attractive  one,  and  seems  a  priori  probable.* 
It  is  conceivable  that  there  may  be,  or  may  have  been,  organisms  where 
it  is  applicable  throughout.  But  an  objective  study  of  the  behavior  of 
Amoeba  shows  that  it  gives  by  no  means  an  adequate  explanation  of 
food-taking  in  this  animal.  As  I  have  shown  in  the  descriptive  por- 
tion, in  Amoeba  proteus  and  A.  angidata  the  food  in  most  cases  is  far 
from  adhering  to  the  protoplasm  ;  on  the  contrary,  it  rolls  away  when 
the  Amoeba  comes  in  contact  with  it,  and  it  is  often  only  as  a  result  of 
long-continued  effort  that  the  animal  succeeds  in  ingesting  it.  The 
first  act  in  ingestion  consists  in  sending  out  pseudopodia  on  each  side  of 
the  mass  to  overcome  the  mechanical  difficulty  resulting  from  the  fact 
that  the  body  does  7iot  adhere  to  the  protoplasm,  but  tends  to  roll  away. 

Further,  a  quantity  of  water  is  usually,  or  frequently,  taken  in  with 
the  food,  and  the  latter  floats  about  in  a  cavity  after  it  is  ingested,  show- 
ing no  tendency  to  adhere  to  the  protoplasm  (see  Leidy,  1S79,  numer- 
ous figures  of  food  vacuoles,  etc.,  and  Le  Dantec,  1S94).  A  similar 
condition  of  affairs  is  shown  in  the  account  of  the  feeding  of  one 
Amoeba  on  another,  given  on  page  201  of  the  present  paper.  Here  the 
prey  does  not  adhere  to  the  protoplasm  of  its  captor,  but  moves  about 
within  the  latter  and  escapes  repeatedly. 

Thus,  in  these  species,  the  taking  of  food  and  the  choice  of  food  can- 
not be  explained  by  the  adherence  of  the  protoplasm  to  the  food  sub- 
stance, for  the  lack  of  such  adherence  is  strikingly  evident. 

Rhumbler's  studies  of  food  taking  were  made  chiefly  on  Amoeba 
verrucosa.  In  this  species  and  its  close  relatives  there  is  much  more 
tendency  for  foreign  objects  to  cling  to  the  surface  than  in  the  other 
species.  But  this  adhesiveness  applies  to  other  objects  as  well  as  to 
food.  It  is  of  special  aid,  as  we  have  seen,  in  tracing  surface  move- 
ments (p.  140).  Particles  of  soot  and  various  other  indifferent  bodies 
stick  to  the  surfoce,  rendering  its  movements  apparent.  Not  all  such 
adhering  bodies  are  taken  into  the  interior,  so  that  the  ingestion 
involves  an  additional  reaction,  and  is  not  fully  accounted  for  by  the 
adhesion  even  in  these  species. 

Rhumbler  has  given  an  ingenious  physical  analysis  of  the  rolling  up 
and  taking  in  of  filaments  of  Oscillaria  by  Amceba  verrucosa^  and  has 
illustrated  the  process  as  he  conceives  it  to  occur  by  a  very  striking 
experiment  (1S98,  p.  330).  A  chloroform  drop  brought  in  contact 
with  the  middle  of  a  filament  of  shellac  rolls  the  filament  together  and 
encloses  it.  Rhumbler  conceives  the  forces  at  work  in  rolling  up  the 
filament  to  be  essentially  the  same  in  the  chloroform  drop  and  in  the 
Amceba.     In  both  cases,  according  to  Rhumbler,  the  surface  tension  of 

♦See  Jennings,  1902,  where  I  adopted  this  view  before  having  investigated  for 
myself  the  behavior  of  Amoeba. 


224  '^^^   BEHAVIOR    OF   LOWER   ORGANISMS. 

the  drop  pulls  on  the  filament,  tending  to  force  it  inward  from  both 
directions.  That  part  of  the  filament  within  the  drop  becomes  softened 
by  the  action  of  the  fluid ;  it,  therefore,  yields  to  the  thrust  from  both 
directions,  and  bends,  permitting  more  of  the  filament  to  be  brought 
into  the  drop  by  the  action  of  surface  tension.  (For  full  explanation, 
see  the  original.) 

It  is  necessary  to  point  out  that  the  explanation  of  the  rolling  up  of 
the  shellac  filament  given  by  Rhumbler  is  erroneous.  The  surface 
tension  of  the  drop,  with  its  inward  thrust,  has  nothing  to  do  with  the 
process,  for  the  filament  is  rolled  up  in  exactly  the  same  manner  when 
it  is  completely  submerged  in  a  large  vessel  of  chloroform,  so  that  it  is 
not  in  contact  with  the  surface  film  at  all.  The  rolling  up  is  evidently 
due  in  some  way  to  the  strains  within  the  shellac  filament,  produced 
when  it  was  drawn  out,  and  to  the  adhesiveness  of  its  surface  when 
acted  upon  by  the  chloroform.  The  process  thus  loses  all  similarity 
to  the  rolling  up  of  the  alga  filament  by  Amoeba.  The  coil  formed  is 
just  as  small  and  close,  and  the  filament  remains  a  filament  just  as  long 
when  the  experiment  is  tried  in  a  large  vessel  of  chloroform  as  when 
only  a  drop  is  used,  as  in  Rhumbler's  experiments. 

Rhumbler's  explanation  of  the  way  in  which  Amoeba  rolls  up  the 
Oscillaria  filament  may,  of  course,  still  be  correct,  though  the  physical 
experiment  by  which  he  attempted  to  illustrate  it  has  nothing  to  do 
with  the  matter.  There  are  certain  points  in  his  description  of  the  pro- 
cess as  it  occurs  in  Amoeba,  however,  that  might  easily  be  interpreted 
in  another  manner.  Such  a  bending  over  of  the  pseudopodium  as  is 
shown  in  Rhumbler's  Fig.  58  (/.  c,  p.  233)  is  not  called  for  by  the 
surface-tension  theor}'.  Rhumbler  holds  that  this  bending  of  the  pseu- 
dopodium is  passive,  and  due  to  the  bending  of  the  filament  within  the 
body(/.  c.,p.  233).  In  view  of  what  we  have  shown  above  (pp.  177-179) 
as  to  the  power  of  active  bending  in  the  pseudopodia,  and  as  to  active 
contractions  of  parts  of  the  ectosarc  in  this  same  species  (pp.  179,  iSo), 
one  might  be  inclined  to  believe  rather  that  this  bending  of  the  pseu- 
dopodium is  active  and  plays  an  important  part  in  bringing  the  fila- 
ment into  the  body.  Rhumbler's  figures  (Fig.  50)  would  support  this 
view  fully  as  strongly  as  his  own  theory,  though  this  would,  of  course, 
not  give  us  a  simple  physical  explanation  of  the  ingestion  of  the  filament. 

Altogether,  we  must  conclude  that  adhesion  between  the  protoplasm 
and  the  food  substance  cannot  by  any  means  give  us  a  general  explana- 
tion of  food-taking  in  Amoeba.  In  some  cases  the  ingestion  of  food 
is  aided  by  such  adhesion,  but  in  other  cases  the  adhesion  is  conspicu- 
ously absent.* 


♦  For  further  confirmation  of  last  stated  fact,  see  paper  of  Le  Dantec  ('1894). 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  225 

GENERAL   CONCLUSION. 

Putting  all  our  results  together,  we  must  conclude  that  the  move- 
ments and  reactions  of  Amoeba  have  as  yet  by  no  means  been  resolved 
into  their  physical  components.  Amoeba  is  a  drop  of  fluid  which 
moves  in  its  usual  locomotion  in  much  the  same  way  as  inorganic  drops 
move  under  the  influence  of  similarly  directed  forces.  But  what  these 
forces  are  is  by  no  means  clear.  When  we  take  into  considera- 
tion the  currents  as  they  actually  exist,  local  decrease  in  surface  tension 
breaks  down  completely  as  an  explanation  for  the  locomotion  and  other 
movements.  The  locomotion  taken  by  itself  might  be  explained  as  due 
to  the  adhesion  of  the  fluid  protoplasm  to  solids,  taken  in  connection 
with  the  surface  tension  of  the  fluid,  but  this  explanation  fails  when  we 
consider  the  formation  of  free  pseudopodia,  and  discover  that  all  the 
processes  concerned  in  locomotion  can  take  place  without  adhesion  to 
the  substratum. 

For  the  reactions  to  stimuli  we  find  a  parallel  condition  of  aflJairs. 
The  currents  in  the  protoplasm  in  the  positive  and  negative  reactions 
are  not  similar  to  those  produced  in  the  attraction  or  repulsion  of  drops 
of  fluid  by  the  direct  action  of  external  agents.  Therefore  we  cannot 
consider  these  reactions  as  due  to  the  increase  or  decrease  of  surface 
tension*  produced  by  the  direct  (or  even  indirect)  action  of  the  external 
agents.  The  taking  and  choice  of  food  cannot  be  physically  explained 
in  any  general  way  by  the  physical  adherence  of  the  protoplasm  as  a 
substance  to  the  food  as  a  substance,  for  food  is  taken  in  many  cases 
(usually,  in  some  species)  where  it  is  demonstrable  that  no  such 
adherence  exists. 

While  we  must  agree  that  Amoeba,  as  a  drop  of  fluid,  is  a  marvel- 
lously simple  organism,  we  are  compelled,  I  believe,  to  hold  that  it  has 
many  traits  which  are  comparable  to  the  "reflexes"  or  *' habits"  of 
higher  organisms. f     We  may,  perhaps,  have  faith  that  such  traits  are 

*It  should  be  pointed  out  that  this  and  other  statements  concerning  surface 
tension  in  Amceba  apply  to  the  tension  of  the  actual  body  surface,  comparing 
Amoeba  thus  to  a  drop  of  simple  fluid.  This  is  the  basis  on  which  rest  the  pre- 
vailing theories  that  would  explain  the  movements  of  Amoeba  by  surface  tension. 
It  is  these  theories  which  I  desired  to  test.  There  remains  untouched,  of  course, 
the  possibility  that  the  movements  of  all  sorts  of  protoplasmic  masses  may  be 
explained  by  changes  in  the  surface  tension  of  the  meshes  of  Blitschli's  honey- 
comb structure,  in  the  manner  indicated  by  BUtschli  (1892,  p.  208).  But  this  is 
at  present  merely  a  hypothesis,  not  worked  out  and  not  controllable  by  observa- 
tion. To  attempt  to  maintain  it  for  Amoeba  would  be  to  relegate  the  movements 
of  this  animal  to  the  same  obscure  category  as  the  movements  of  cilia  and  of 
muscles,  possibly  a  correct  proceeding,  but  removing  the  matter  at  present  from 
the  field  of  experimental  observation. 

t  See  the  next  division  of  this  paper,  wheie  this  point  is  developet}. 


226  THE  BEHAVIOR    OF    LOWER    ORGANISMS. 

finally  resolvable  into  the  action  of  chemical  and  physical  laws,  but  we 
must  admit  that  we  have  not  arrived  at  this  goal  even  for  the  simpler 
activities  of  Amoeba. 

THE  BEHAVIOR  OF  AMCEBA  FROM  THE  STANDPOINT  OF  THE 
COMPARATIVE  STUDY  OF  ANIMAL  BEHAVIOR. 

HABITS     IN   AMCEBA. 

Although  in  general  Amoeba  has  the  rolling  movement  of  a  drop  of 
fluid,  yet  this  statement  by  no  means  brings  out  all  the  characteristics 
of  the  movement  in  any  given  species  of  Amoeba.  Different  kinds  of 
Amoebae  move  differently,  and  the  differences  are  in  many  cases  not 
such  as  can  be  accounted  for  by  differences  in  the  state  of  aggregation 
of  the  body  substance.  Some  Amoebae,  as  is  well  known,  form  many 
pseudopodia,  others  few  or  none.  Different  Amoebae  have  different 
characteristic  forms  in  locomotion.  But  more  striking  than  these  gen- 
erally recognized  peculiarities  are  certain  others  of  a  more  special  char- 
acter. A  creeping  Amoeba  angulata^  as  we  have  seen  above,  frequently 
pushes  upward  and  forward  at  the  anterior  end  a  short,  acute  pseudo- 
podium,  which  waves  slightly  from  side  to  side  like  an  antenna  (p.  177 
and  Fig.  62,  c).  This  peculiar  habit  is  much  more  pronounced  in 
Amoeba  velata  Parona,  according  to  Penard  (1902).  In  this  animal 
the  free  anterior  pseudopodium  may  extend  for  a  length  greater  than 
the  diameter  of  the  body  ;  Penard  compares  it  directly  to  a  tentacle. 
Some  other  species  of  Amoeba  never  send  forward  such  an  antenna-like 
pseudopodium.  The  great  work  of  Penard  (/.  c.)  contains  innumer- 
able instances  of  such  peculiarities  of  form,  movement,  and  function 
among  the  different  species  of  Amoeba  and  other  Rhizopods  ;  some  of 
them  are  collected  in  that  author's  interesting  section  on  the  pseudo- 
podia (/.  c,  pp.  625-629).  It  is  not  necessary  to  take  these  up  in  detail 
here.  The  point  of  interest  is  that  different  sorts  of  Amoebae  have  dif- 
ferent customary  methods  of  action,  such  as  are  commonly  spoken  of 
as  *'  habits"*  in  higher  animals,  and  that  these  *'  habits"  are  no  more 
easily  explicable  on  direct  physical  grounds  in  Amoeba  than  in  higher 
animals.  Let  anyone  attempt,  for  example,  to  explain  from  the 
physics  of  viscous  fluids  why  Afnoeba  velata  or  A,  angulata  push 
out  an  antenna-like  pseudopodium  at  the  anterior  end  and  wave  it  from 
side  to  side,  while  Amoeba  proteus  and  A.  Umax  do  not. 


♦The  word  habit  is,  of  course,  not  used  here  of  a  method  of  action  acquired 
during  the  life  of  the  individual,  but  merely  of  a  fixed  method  of  behavior.  At 
all  events,  it  is  difficult  to  distinguish  between  these  two  things  where  individual 
organisms,  as  in  Amoeba,  have  lived  as  long  as  the  race. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA. 


227 


CLASSES    OF   STIMULI   TO    WHICH    AMCEBA    REACTS. 

The  simple  naked  mass  of  protoplasm  reacts  to  all  classes  of  stimuli 
to  which  higher  animals  react  (if  we  consider  the  auditory  stimulus 
merely  a  special  case  of  the  mechanical  stimulus).  Mechanical  stimuli, 
chemical  stimuli,  temperature  differences,  light,  and  electricity — all 
control  the  direction  of  movement,  as  they  do  in  higher  animals. 

TYPES    OF    REACTION. 

Amoeba  has  two  chief  types  of  reaction,  by  one  or  the  other  of  which 
it  responds  to  most  stimuli.  These  we  may  call  the  positive  and  the 
negative  reactions.  As  a  third  type  we  must  distinguish  the  food 
reaction,  which  cannot  be  brought  completely  under  either  of  the  two 
chief  types  of  reaction  above  mentioned. 

(i)  The  positive  reaction  consists  in  pushing lout  the  body  substance 
toward  the  source  of  stimulus  and  rolling  in  that  direction. 

(2)  The  negative  reaction  consists  in  withdrawal  of  body  substance 
and  rolling  in  some  other  direction — not  necessarily  in  the  opposite 
direction. 

(3)  The  food  reaction  is  not  sharply  definable.  Its  most  character- 
istic features  consist  in  the  hollowing  out  of  the  anterior  end  and  in 
the  pushing  out  of  pseudopodia  at  each  side  of  and  over  the  food  body. 
It  involves  also  the  positive  reaction  above  characterized. 

RELATION    OF    THE     DIFFERENT    REACTIONS    TO    DIFFERENT    STIMULI  ; 
ADAPTATION    IN    THE    BEHAVIOR    OF    AMCEBA. 

(a)  The  positive  reaction  is  known  to  be  produced  by  weak  mechanical 
stimuli ;  it  is  probably  produced  also  by  weak  chemical  stimuli  (in  the 
reactions  to  food,  pp.  193-202).  The  positive  reaction  to  weak  mechan- 
ical stimuli  serves  the  purpose  of  bringing  the  floating  animal  to  a  sur- 
face on  which  it  can  creep.  The  positive  reaction  to  food  substances 
(mechanical  and  chemical  stimuli),  of  course,  serves  to  obtain  food. 
The  positive  reaction  is  thus,  as  a  rule,  performed  under  such  circum- 
stances as  to  be  beneficial  to  the  organism  ;  i.  e.,  it  is  directly  adaptive. 

(3)  The  negative  reaction  is  produced  by  powerful  stimuli  of  all 
sorts.  Such  powerful  stimuli  are,  as  a  rule,  injurious,  and  the  nega- 
tive reaction  tends  to  remove  the  Amoeba  from  their  action  ;  it  is,  there- 
fore, directly  adaptive.  This  is  true  of  the  negative  reaction  to  light 
as  well  as  to  other  stimuli,  for  light  is  known  to  interfere  with  the  activi- 
ties of  Amoeba.  The  reaction  to  the  electric  current  is  of  exactly  the 
character  that  would  be  produced  by  a  strong  stimulus  on  the  anode 
side,  but  owing  to  the  peculiarity  of  the  current  the  reaction  does  not 
assist  the  Amoeba  to  escape.  The  reaction  to  the  electric  current  can 
not  then  be  considered  adaptive  ;  this  stimulus  forms,  of  course,  no 
part  of  the  normal  environment  of  an  Amoeba. 


228  THE    BEHAVIOR    OF    LOWER    ORGANISMS. 

The  method  by  which,  throuj^h  the  negative  reaction,  Amoeba  avoids 
an  injurious  agent  is  of  interest.  The  animal  does  not  go  directly  away 
from  the  injurious  agent,  as  by  moving  toward  the  side  opposite  that 
stimulated.  It  moves  in  any  direction  except  toward  the  region  stimu- 
lated. There  is  no  system  of  conduction  such  that  strong  stimulation  in 
a  given  spot  involves  movement  directed  toward  the  opposite  side.  If 
the  movement  in  the  new  direction  induces  a  new  stimulation,  the  direc- 
tion is  again  changed.  This  may  be  continued  until  the  original  direction 
of  movements  is  squarely  reversed.  The  method  is  akin  to  that  of  trial 
and  error  in  higher  organisms  (see  Morgan,  1894,  pp.  241-242). 

(c)  The  food  reaction  is  directly  adaptive  in  that  it  procures  food. 
As  a  rule  this  reaction  occurs  only  when  the  source  of  stimulation  is 
fitted  to  serve  as  food.  Empty  diatom  shells,  sand  grains,  debris,  etc., 
are,  as  a  rule,  not  taken  into  the  body,  as  many  observers  have  pointed 
out.  Sometimes  material  is  taken  into  the  body  that  is  not  useful,  as 
is  described  by  Rhumbler  (189S,  p.  236).  In  such  cases  there  is  no 
evidence  of  a  food  reaction  in  the  sense  characterized  above;  the 
material  is  ingested  accidentally^  as  it  were,  through  its  adherence  to 
the  protoplasm.  The  food  reaction,  as  a  definite  form  of  behavior,  is 
always  adaptive  so  far  as  known. 

{d)  Some  of  the  habits  of  Amoeba,  characterized  above,  are  clearly 
adaptive.  The  use  of  the  antenna-like  pseudopodium  sent  out  by 
Ammba  velata  and  A.  angulata  is  evident.  Penard  describes  in  detail 
how  Ammba  velata  .uses  it  in  pafssing  from  one  substratum  to  another. 

The  habit  which  some  Amoebae  have,  when  suspended  freely  in  the 
water,  of  sending  out  pseudopodia  in  all  directions  (p.  iSi)  is,  of  course, 
useful  in  that  it  increases  the  chances  of  coming  in  contact  with  some 
solid  object,  without  which  the  Amoeba  cannot  move  from  place  to 
place. 

REFLEXES    AND    '^  AUTOMATIC    ACTIONS  "    IN    AMCEBA. 

In  the  behavior  of  Amoeba  we  can  distinguish  factors  directly  com- 
parable to  the  reflexes  and  *' automatic  activities  "  of  higher  organisms. 
The  responses  of  Amoeba  to  stimuli  have  the  nature  of  reflexes  in  the 
fact  that  they  are  not  direct  effects  of  the  physical  action  of  the  stimulus 
(see  p.  219),  but  are  determined  by  the  internal  conditions  of  the 
organism.  They  may  be  called  reflexes,  unless  we  propose,  as  certain 
writers  do,  to  restrict  the  term  reflex  to  processes  involving  differen- 
tiated nerves.  The  precise  designation  is  unimportant ;  the  essential 
point  is  that  the  responses  agree  with  the  reflexes  of  higher  animals  in 
being  indirect. 

Ziehen,  in  his  Leitfaden  der  physiologischen  Psychologic  (sixth 
edition,  p.  10),  defines  as  automatic  acts  '•  motor  reactions,  which  do 


THE    MOVEMENTS    AND    REACTIONS    OF    AMCEBA.  229 

not,  like  the  reflexes,  follow  unchangeably  upon  a  definite  stimulus, 
but  which  are  modified  in  their  course  by  new,  intercurrent  stimuli." 
In  this  sense  Amoeba,  of  course,  shows  automatic  behavior.  Its 
responses  are  by  no  means  unchangeably  fixed  ;  on  the  contrary,  its 
behavior  is  often  modified  by  the  slightest  change  in  the  stimulus  to 
which  it  is  reacting.  For  examples  of  this  see  the  chase  of  one  Amoeba 
by  another  (p.  200),  the  following  of  a  rolling  ball  of  food  (p.  196),  the 
account  of  the  driving  of  Amoeba  (p.  185),  and  the  description  of  the 
method  by  which  Amoeba  avoids  an  obstacle  (p.  186). 

Whether  these  actions  agree  with  the  accepted  idea  of  an  automatic 
action  in  being  unconscious  we  have,  of  course,  no  means  of  knowing. 

VARIABILITY    AND    MODIFIABILITY    OF    REACTIONS. 

There  is  little  that  can  be  said  on  this  point.  Verworn  (1890,  «,  p. 
271)  says  that  when  an  electric  current  is  passed  through  a  prepara- 
tion containing  many  Amoebae,  some  Vespond  strongly,  while  others 
do  not ;  thus  different  individuals  vary  in  their  responsiveness.  Fur- 
ther, a  given  individual  may  become  accustomed  to  the  current,  at  first 
responding  to  it,  later  not  responding.  Doubtless  such  phenomena  of 
acclimation  are  common  in  the  reactions  to  all  sorts  of  stimuli. 

Rhumbler  (1898,  p.  203)  shows  that  when  Amoebae  are  engaged  in 
taking  Oscillaria  filaments  as  food,  light  thrown  upon  them  modifies 
them  physiologically  in  such  a  way  that  they  eject  the  food.  The 
nature  of  the  reaction  is  thus  shown  to  depend  partly  on  the  physio- 
logical condition  of  the  animal. 

There  is  no  direct  experimental  evidence  as  yet,  so  far  as  I  am  aware, 
that  Amoeba  shows  memory.*  Experimental  evidence  as  to  whether 
the  reactions  of  a  given  Amoeba  to  a  given  stimulus  are  modified  by 
previous  stimuli  received  is  very  difficult  to  obtain,  principally  because 
it  is  practically  impossible  to  make  succeeding  stimuli  alike,  so  that 
one  cannot  tell  whether  a  difference  in  the  reaction  is  due  to  a  differ- 
ence in  the  present  stinnilus  or  not.  Possibly  there  is  a  faint  indication 
of  something  akin  to  memory  shown  in  the  facts  described  on  page  201. 
Here  a  smaller  Amoeba  which  had  been  ingested  as  prey  escaped  from 
the  posterior  end  of  the  captor  ;  the  latter  tliereupon  reversed  its  move- 
ments, came  up  with  the  escaping  prey,  and  again  ingested  it.  In  the 
interval  between  the  complete  separation  of  the  prey  from  its  captor 
and  its  recapture,  the  behavior  of  the  captor  would  seem  to  have  been 
determined  by  some  trace  left  within  it  by  the  former  possession  of  the 

♦The  word  memory  is,  of  course,  used  here  of  the  objective  phenomenon  that 
in  many  animals  present  behavior  is  modified  in  acconlance  with  past  stimuli 
received,  or  past  reactions  given.  Of  possible  subjective  accompaniments  of  this 
objective  phenomenon  we,  of  course,  know  nothing  directly  so  far  as  the  lower 
organisms  are  concerned. 


230  THE    BEHAVIOR   OF   LOWER   ORGANISMS. 

prey.  But,  possibly,  this  trace  was  merely  of  a  gross  physical  char- 
acter, acting  as  a  direct  stimulus  to  produce  the  observed  behavior.  If 
this  is  true,  the  behavior  shows  no  indication  of  memory. 

SUMMARY. 

OBSERVATIONS. 
THE   USUAL   MOVEMENTS. 

(i)  Locomotion  in  Amoeba  is  a  process  that  may  be  compared  with 
rolling,  the  upper  and  lower  surfaces  continually  interchanging  posi- 
tions. This  is  shown  by  observation  of  the  movements  of  particles 
attached  to  the  outer  surface  or  embedded  in  the  ectosarc  of  the  animal. 
Such  attached  particles  move  forward  on  the  upper  surface  and  over 
the  anterior  edge,  remain  quiet  on  the  under  surface  till  the  body  of  the 
Amoeba  has  passed,  then  pass  upward  at  the  posterior  end  and  forward 
on  the  upper  surface  again.  Single  particles  may  thus  be  observed  to 
make  many  complete  revolutions.  (See  p.  170,  Fig.  58,  and  Figs.  38, 39, 
40,  41.)  * 

(2)  Thus  the  upper  surface  moves  forward  in  the  same  direction  as 
the  internal  currents,  while  the  lower  surface  is  at  rest.  There  is  char- 
acteristically no  backward  current  anywhere  in  Amoeba,  though  at 
times  some  of  the  endoplasmic  particles,  spreading  out  laterally  at  the 
anterior  end,  may  move  a  slight  distance  backward  at  the  sides.  This 
is  rare  (see  p.  134).  The  forward  current  on  the  upper  surface  is  not 
confined  to  a  thin  layer,  but  extends  inward  to  the  endosarc  ;  the  endo- 
sarcal  and  surface  currents  are  one  (p.  142). 

(3)  In  the  formation  of  pseudopodia  that  are  in  contact  with  the 
substratum  the  movement  of  protoplasm  is  identical  with  that  at  the 
anterior  end  of  the  Amoeba.  The  upper  surface  and  internal  contents 
flow  toward  the  tip,  while  the  surface  in  contact  with  the  substratum  is 
quiet.  Particles  adhering  to  the  upper  surface  are  carried  out  to  the  tip 
and  rolled  under  to  the  lower  surface,  where  they  remain  quiet  (p.  152). 

(4)  In  the  formation  of  pseudopodia  projecting  freely  into  the  water, 
the  movements  of  substance  are  the  same  as  in  pseudopodia  that  are  in 
contact,  save  that  there  is  no  part  of  the  surface  at  rest.     The  whole 

♦  Of  anyone  who  is  inclined  to  reject  these  results  on  the  basis  of  previous 
observations,  or  of  their  supposed  incompatibility  with  other  known  facts,  let 
me  make  the  following  request :  Before  taking  ground  against  the  results,  pro- 
cure some  specimens  of  Amoeba  verrucosa  or  one  of  its  relatives.  This  is  usually 
easily  done.  Then  mix  thoroughly  with  the  water  containing  them  some  fine 
soot,  and  observe  carefully  the  movements  of  the  animals.  The  particles  attach 
themselves  to  the  outside,  and  the  movements  of  the  surface  are  then  observable 
with  the  greatest  ease.  It  is  such  a  simple  matter  to  determine  certain  of  the 
chief  points  for  one's  self  in  this  manner  that  it  would  be  regrettable  for  contro- 
versy to  arise  through  neglect  of  the  needed  observations. 


THE    MOVEMENTS    AND    REACTIONS    OF   AMCEBA.  23 1 

surface  thus  moves  outward,  and  new  parts  of  the  surface  of  the  body 
continually  pass  on  to  the  pseudopodium.  An  object  adhering  to  the 
surface  of  the  pseudopodium  remains  at  approximately  the  same  dis- 
tance from  the  tip,  both  when  the  pseudopodium  is  short  and  when  it 
has  become  very  long  (pp.  153-156,  and  Figs.  47-49). 

(5)  In  the  withdrawal  of  a  free  pseudopodium  (a)  a  process  occurs 
that  is  the  reverse  of  that  described  in  (4),  the  surface  of  the  pseudo- 
podium passing  from  its  base  on, to  the  surface  of  the  body  (p.  156, 
and  Fig.  49) ;  (6)  the  surface  of  the  pseudopodium  becomes  wrinkled 
and  shrunken  ;   (c)  the  endosarc  flows  back  into  the  body. 

(6)  Any  part  of  the  protoplasm  may  be  excluded  temporarily  from 
the  forward  currents.  In  many  Amoebae  there  is  usually  a  region  at 
the  posterior  end  which  is  thus  temporarily  excluded  (the  posterior 
appendage,  tail).  In  such  cases  the  lower  surface  of  the  Amoeba 
passes  upward  on  each  side  of  this  appendage  to  become  part  of  the 
upper  surface,  then  passes  forward  (p.  169,  and  Fig.  57).  The  sub- 
stance of  the  posterior  appendage  is  itself  gradually  drawn  into  the 
forward  current. 

(7)  The  anterior  portion  of  the  advancing  Amoeba  is  attached  to  the 
subvStratum,  while  the  posterior  portion  is  not  (p.  165).  There  is  a  viscid 
secretion  produced  on  the  outer  surface  of  the  Amoeba,  to  which  the 
attachment  may  be  due. 

(8)  The  attached  anterior  portion  of  the  body  is  spread  out  and 
usually  very  thin.  The  unattached  posterior  portion  becomes  rounded 
and  thick,  and  is  contracting,  so  that  there  is  a  slight  forward  move- 
ment on  the  lower  surface,  as  well  as  on  the  upper  surface,  in  this  part 
(p.  166). 

(9)  All  the  activities  concerned  in  locomotion  can  be  performed  when 
the  animal  is  not  attached  to  the  substratum.  (But  for  progression  such 
attachment  is  necessary,  p.  215.) 

(10)  The  locomotion  of  Amoeba  is  similar  even  in  details  to  the 
movements  of  a  drop  of  inorganic  fluid  which  adheres  strongly  to  the 
substratum  at  one  edge  and  spreads  out  upon  it  here,  while  the  other 
edge  is  free  (pp.  209-214).  It  is  similar  in  most  respects  (except  in  the 
thinness  of  the  anterior  edge)  to  the  movements  under  the  influence  of 
gravity  of  a  drop  of  fluid  along  an  inclined  surface  to  which  it  adheres 
but  slightly. 

(11)  The  currents  in  a  moving  Amoeba  are  not  similar  to  those  of  a 
drop  of  inorganic  fluid  that  is  moving  or  elongating  as  a  result  of  a  local 
increase  or  decrease  in  surface  tension.  The  surface  currents  away 
from  the  region  of  least  tension  and  in  the  opposite  direction  to  the 
axial  currents  that  are  characteristic  of  such  a  drop  are  lacking  in 
Amoeba.  Here  surface  and  axial  currents  have  the  same  direction 
(p.  205). 


332  THE    BEHAVIOR    OF    LOWKR    ORGAKISMS. 

(12)  Similarly,  the  movements  of  material  in  a  forming  pseudo- 
podium  are  not  like  those  in  a  projection  which  is  produced  in  a  drop 
of  inorganic  fluid  as  a  result  of  a  local  decrease  in  surface  tension.  The 
surface  currents  away  from  the  tip  in  the  inorganic  projection  are  lack- 
ing in  Amoeba,  the  surface  here  moving  in  the  same  direction  as  the 
tip  (p.  206). 

(13)  The  body  of  Amoeba  shows  under  some  conditions  elasticity 
of  form,  such  as  is  characteristic  of  solids  (pp.  175-177). 

(14)  Besides  the  movements  directly  concerned  in  the  usual  loco- 
motion, limited  local  contractions  may  occur,  resulting  in  swinging  or 
vibratory  motions  of  the  pseudopodia  (p.  177),  or  in  sudden,  jerky 
movements  of  the  body  as  a  whole  (p.  179),  or  in  the  constricting  off" 
of  parts  of  the  body  (p.  180). 

(15)  The  roughness  of  surface  in  a  retracting  pseudopodium,  the 
retention  of  irregular  forms  by  Amoeba,  and  the  movements  mentioned 
in  the  foregoing  paragraph,  are  similar  to  certain  phenomena  to  be 
observed  in  mixtures  of  solids  and  fluids,  as  a  result  of  the  interaction 
of  surface  tension  and  the  friction  of  the  solid  particles  (p.  215). 

REACTIONS    TO    STIMULI. 

(16)  The  following  reactions  are  described :  Positive  and  negative 
reactions  to  mechanical  stimuli  (pp.  1S1-187) ;  negative  reactions  to 
chemical  stimuli  (pp.  1S7-190);  negative  reaction  to  heat  (pp.  190-191); 
reaction  to  the  constant  electric  current  (pp.  1 91-192);  complex  reac- 
tions connected  with  food-taking  (pp.  193-202);  reactions  to  injuries 
(pp.  202-204). 

(17)  In  most  reactions  modifying  the  direction  of  motion  a  new 
advancing  wave  of  protoplasm  is  sent  out  from  some  part  of  that  por- 
tion of  the  body  which  is  already  attached  to  the  substratum.  The 
internal  and  surface  currents  then  flow  in  that  direction,  thus  changing 
the  course  of  the  animal.  Thus,  when  the  animal  changes  its  course  in 
a  reaction,  the  surface  currents  change  their  course  in  a  corresponding 
way,  as  shown  by  the  movements  of  particles  on  the  surface  (pp.  143, 
185,  192). 

(18)  Sometimes  the  course  is  squarely  reversed  as  a  result  of  a 
stimulus.  In  this  case  the  original  anterior  region  becomes  detached 
from  the  bottom,  while  a  new  pseudopodium  projects  freely  into  the 
water  from  the  former  posterior  (unattached)  region,  settles  down,  and 
becomes  attached ;  the  internal  and  surface  currents  then  follow  it. 
This  process  requires  usually  a  considerable  interval  of  time  (pp.  183, 
1S4). 

(19.)  Both  surface  currents  and  internal  currents  are  toward  the 
source  of  stimulation  in  a  positive  reaction,  away  from  the  source  of 
stimulation  in  a  negative  reaction. 


THE    MOVEMENtS    AND   tlEACTlONS   OF  AMOEBA.  2'^^'^ 

(20)  The  currents  in  the  positive  and  negative  reactions  are  not 
similar  to  the  currents  in  a  drop  of  inorganic  fluid  moving  toward  or 
away  from  an  agent  which  causes  a  local  decrease  or  increase  in  the 
surface  tension.  In  Amoeba  the  currents  on  the  surface  and  in  the 
interior  are  congruent ;  in  the  inorganic  fluid  they  are  opposed. 

(21)  In  the  taking  of  food  the  protoplasm  and  the  food  body  in 
many  cases  do  not  tend  to  adhere,  so  that  the  Amoeba  is  compelled  to 
overcome  considerable  mechanical,  difliculty  before  the  food  can  be 
inclosed.  Frequently  the  food  body  rolls  away  from  the  animal  as  soon 
as  it  is  touched  (pp.  193,  196).  The  difficulty  is  overcome  by  sending 
out  pseudopodia  on  each  side  of  the  body  and  inclosing  it,  together  with 
a  certain  amount  of  water.  In  A?nceba  verrucosa  and  its  relatives  food- 
taking  is  aided  by  the  tendency  of  foreign  bodies  to  adhere  to  the  body 
surface.  Amoebae  frequently  prey  upon  each  other,  and  this  often  gives 
rise  to  a  long  and  complex  train  of  reactions  (pp.  198-202,  and  Fig.  76). 

CONCLUSIONS. 

(22)  The  chief  factors  in  locomotion  seem  to  be  as  follows:  (i)  At 
the  anterior  edge  of  the  Amoeba  a  wave  of  protoplasm  pushes  out,  rolls 
over,  and  becomes  attached  to  the  substratum ;  (2)  This  pulls  on  the 
upper  surface  of  the  Amoeba,  causing  it  to  move  forward ;  (3)  The 
hinder  portion  of  the  Amoeba  becomes  released  from  the  substratum, 
and  contracts  slowly  ;  (4)  As  a  result  of  the  strong  pull  from  in  front 
and  the  slight  contraction  from  behind  the  posterior  end  moves  forward  ; 
(5)  The  internal  substance  must  flow  forward  as  a  result  of  the  pull  on 
the  upper  surface,  the  movement  forward  of  the  posterior  end,  and  the 
pressure  due  to  the  pulling  from  in  front  and  the  contraction  behind. 
The  movement  of  the  internal  fluid  is  comparable  to  that  in  a  sac  or 
bladder  half  filled  with  water  and  rolled  along  a  surface  (pp.  146,  149, 
171). 

(23)  There  is  no  continuous  transformation  of  endosarc  into  ectosarc 
at  the  anterior  end,  and  of  ectosarc  into  endosarc  behind  this  (Rhum- 
bler's  ento-ectoplasm  process),  as  a  necessary  feature  of  locomotion, 
since  the  ectosarc  of  the  upper  surface  rolls  over  to  the  under  surface 
at  the  anterior  end  (p.  148).  Nevertheless,  ectosarc  and  endosarc  are 
mutually  interconvertible  when  need  arises  for  the  change  of  one  into 
the  other. 

(24)  It  results  from  paragraphs  (i),  (2),  (11),  above,  that  the  loco- 
motion of  Amoeba  cannot,  with  fidelity  to  the  results  of  the  physical 
experiments,  be  accounted  for  by  a  decrease  in  surface  tension  at  the 
anterior  end. 

(25)  From  (3),  (4),  (12),  above,  we  must  conclude  that  the  sending 
out  of  pseudopodia  cannot,  without  violence  to  the  results  of  the  phys- 
ical experiments,  be  accounted  for  as  due  to  a  local  decrease  in  surface 
tension  at  the  point  of  the  pseudopodium. 


334  '^^^   BEHAVIOR   OF   LOWER   ORGANISMS. 

(26)  From  (i)  and  (10)  above  it  results  that  the  simple  locomotion 
on  a  substratum  could,  taken  by  itself,  be  accounted  for  on  Berthold's 
theory  that  the  movement  is  due  to  the  spreading  out  of  a  fluid  on  a 
solid.  But  this  theory  fails  when  we  take  into  account  the  formation 
of  free  pseudopodia  (p.  214),  and  the  fact  that  all  the  processes  con- 
cerned in  locomotion  can  be  performed  without  adherence  to  a  solid 
(paragraph  (9)  above). 

(27)  From  (3),  (4),  (9),  (11),  (12),  (24),  (25),  (26),  we  must  con- 
clude that  the  formation  of  pseudopodia  and  the  sending  out  of  waves 
of  protoplasm  at  the  anterior  end  of  a  moving  Amoeba  are  due  to  a 
local  activity  of  the  protoplasm  for  which  no  physical  explanation  has 
been  given.  Since  these  are  the  essential  features  in  locomotion,  we 
must  conclude  that  locomotion  in  Amoeba  has  not  been  physically 
explained. 

(28)  From  (17),  (19),  (20),  it  follows  that  we  cannot,  with  fidelity 
to  the  results  of  physical  experimentation,  hold  that  the  effects  of  stimuli 
in  modifying  the  movements  of  Amoeba  are  due  to  their  direct  (or  even 
indirect)  action  in  changing  the  surface  tension  of  the  parts  affected. 

(29)  From  (21)  we  must  conclude  that  adherence  between  the  proto- 
plasm and  the  food  substance  does  not  furnish  an  adequate  explanation 
of  food-taking  and  the  choice  of  food  in  Amoeba. 

(30)  From  (24),  (25),  (27),  (28),  we  must  conclude  that  changes  in 
the  surface  tension  of  the  body  are  not  the  primary  factors  in  the  move- 
ments and  reactions  of  Amoeba.     (See  note,  p.  225). 

(31)  All  the  results  taken  together  lead  to  the  conclusion  that  neither 
the  usual  movements  nor  the  reactions  of  Amoeba  have  as  yet  been 
resolved  into  known  physical  factors.  There  is  the  same  unbridged 
gap  between  the  physical  effect  of  the  stimulus  and  the  reaction  of  the 
organism  that  we  find  in  higher  animals. 

(32)  In  the  behavior  of  Amoeba  we  may  distinguish  factors  compar- 
able to  the  habits,  reflexes,  and  automatic  activities  (Ziehen)  of  higher 
organisms  (pp.  228-229).  Its  reactions  as  a  rule  are  adaptive  (pp. 
227-228). 


SEVENTH    PAPER 


THE  METHOD  OF  TRIAL  AND  ERROR  IN  THE 
BEHAVIOR  OF  LOWER  ORGANISMS. 


235 


THE    METHOD  OF   TRIAL  AND  ERROR    IN  THE 
BEHAVIOR  OF  LOWER  ORGANISMS. 


A  certain  type  of  behavior  in  higher  animals  has  been  characterized 
by  Lloyd  Morgan  as  the  method  of  trial  and  error.  The  nature  of  such 
behavior  is  well  brought  to  mind  by  an  example  from  Morgan  (1894, 
p.  357).  His  dog  v^as  required  to  bring  a  hooked  walking  stick 
through  a  narrow  gap  in  a  fence.  The  dog  did  not  pause  to  consider 
that  the  stick  would  pass  through  the  narrow  opening  only  if  taken 
by  one  end  and  pulled  lengthwise.  On  the  contrary,  he  simply  seized 
the  stick  in  the  way  that  happened  to  be  most  convenient,  near  its 
middle,  and  tried  to  carry  it  through  the  gap  in  the  fence  in  that  man- 
ner. Of  course,  the  stick  would  not  pass,  and  after  some  effort  the 
dog  was  forced  to  drop  it.  Then  he  seized  it  again  at  random,  and 
made  a  new  effort.  Again  the  stick  was  stopped  by  the  fence  ;  again 
the  dog  dropped  it,  took  a  new  hold,  and  tried  again.  After  several 
repetitions  of  this  performance,  the  dog  seized  the  stick  by  the  hooked 
end.     This  time  it  passed  through  the  gap  in  the  fence  easily. 

The  dog  had  '"tried"  all  possible  methods  of  pulling  the  stick 
through  the  fence.  Most  of  the  attempts  showed  themselves  to  be 
*' error."  Then  the  dog  tried  again,  till  lie  finally  succeeded.  Thus 
he  worked  by  the  method  of  trial  and  error. 

This  method  of  reaction  has  been  found  by  Lloyd  Morgan,  Thorn- 
dike  (1S9S),  and  others,  to  play  a  large  part  in  the  development  of 
intelligence  in  higher  animals.  Intelligent  action  arises  as  follows: 
The  animal  works  by  the  method  of  trial  and  error  till  it  has  come 
upon  the  proper  method  of  performing  an  action.  Thereafter  it  begins 
with  the  proper  way,  not  performing  the  trials  anew  each  time.  Thus 
intelligent  action  has  its  basis  in  the  method  of  ''  trial  and  error,"  but 
does  not  abide  indefinitely  in  that  method. 

Behavior  having  the  essential  features  of  the  method  of  '*  trial  and 
error"  is  widespread  among  the  lower  and  lowest  organisms,  though 
it  does  not  pass  in  them  so  immediately  to  intelligent  action.  But  like 
the  dog  bringing  the  stick  through  the  fence  the  first  time,  they  try  all 
ways,  till  one  shows  itself  practicable. 

This  is  the  general  plan  of  behavior  among  the  lowest  organisms 
under  the  action  of  the  stimuli  which  pour  upon  them  from  the  sur- 
roundings. On  receiving  a  stimulus  that  induces  a  motor  reaction, 
they  try  going  ahead  in  various  directions.  When  the  direction  fol- 
lowed leads  to  a  new  stimulus,  they  tr}'  another,  till  one  is  found  which 
does  not  lead  to  effective  stimulation, 

237 


238 


THE  BEHAVIOR  OF  LOWER  ORGANISMS. 


This  method  of  trial  and  error  is  especially  well  developed  in  free- 
swimming  single-cell  organisms — the  flagellate  and  ciliate  infusoria — 
and  in  higher  animals  living  under  similar  conditions,  as  in  the  Roti- 
fera.  In  these  creatures  the  structure  and  the 
method  of  locomotion  and  reaction  are  such 
as  to  seem  cunningly  devised  for  permitting 
behavior  on  the  plan  of  trial  and  error  in  the 
simplest  and  yet  most  effective  way. 

These  organisms,  as  they  swim  through  the 
water,  typically  revolve  on  the  long  axis,  and  at 
the  same  time  swerve  toward  one  side,  which 
is  structurally  marked.  This  side  we  will  call 
X.  Thus  the  path  becomes  a  spiral.  The  or- 
ganism is,  therefore,  even  in  its  usual  course, 
successively  directed  toward  many  different 
points  in  space.  It  has  opportunity  to  try  suc- 
cessively many  directions  though  still  progress- 
ing along  a  definite  line  which  forms  the  axis 
of  the  spiral  (see  Fig.  79).  At  the  same  time 
the  motion  of  the  cilia  by  which  it  swims  is 
pulling  toward  the  head  or  mouth  a  little  of  the 
water  from  a  slight  distance  in  advance  (Fig. 
79).  The  organism  is,  as  it  were,  continually 
taking  "samples"  of  the  water  in  front  of  it. 
This  is  easily  seen  when  a  cloud  of  India  ink 
is  added  to  the  water  containing  many  such 
organisms. 

At  times  the  sample  of  water  thus  obtained  is 
of  such  a  nature  as  to  act  as  a  stimulus  for  a 
motor  reaction.  It  is  hotter  or  colder  than 
usual,  or  contains  some  strong  chemical  in  solu- 
tion, perhaps.  Thereupon  the  organism  reacts 
in  a  very  definite  way.  At  first  it  usually 
stops  or  swims  backward  a  short  distance,  then 
it  swings  its  anterior  end  farther  than  usual 
toward  the  same  side  X  to  which  it  is  al- 
ready swerving.  Thus  its  path  is  changed. 
After  this  it  begins  to  swim  forward  again.  The  amount  of  backing 
and  of  swerving  toward  the  side  X  is  greater  when  the  stimulus  is  more 
intense. 


3 


Fig.  79.* 


♦Fig.  79. — Spiral  path  in  the  ordinary  swimming  of  Paramecium,  showing 
how  the  anterior  end  is  pointed  successively  in  different  directions,  and  how  a 
sample  of  water  is  drawn  to  the  anterior  end  and  mouth  from  each  of  these 
directions. 


THE    METHOD    OF    TRIAL    AND    ERROR. 


239 


This  method  of  reaction  seems  very  set  and  simple  when  considered 
by  itself.  It  is  almost  like  that  of  a  muscle  which  reacts  by  the  same 
contraction  to  all  effective  stimuli.  The  behavior  of  these  animals 
seems,  then,  of  the  very  simplest  character.  To  practically  all  strong 
stimuli  they  react  in  a  single  definite  way. 

But  if  we  look  closely  at  this  simple  method  of  reacting,  we  find  it, 
after  all,  marvelously  effective.     The  organism,  as  we  have  seen,  is 


i^ 


revolving  on  its  long  axis.     When,  as  a  consequence  of  stimulation,  it 
swings  its  anterior  end  toward  the  side  X^  this  movement  is  combined 

♦  Fig.  80  — Diagrams  of  the  movements  in  a  reaction  to  a  stimulus  in  an  infu- 
sorian,  Paramecium  C>4),  and  in  a  rotifer,  Anursea(5),  The  anterior  end  swings 
about  in  a  circle  (turning  continually  toward  the  aboral  or  dorsal  side).  It  thus 
tries  many  different  directions,  at  the  same  time  receiving  samples  of  water  from 
each  of  these  directions,  i,  2,  3,  4,  5,  the  successive  positions  taken,  with  the 
currents  of  water  at  the  anterior  ends.  If  the  stimulus  ceases  the  organism 
may  stop  in  any  of  these  positions,  and  swim  forward  in  the  direction  so  indi- 
cated. (The  backward  swimming,  which  precedes  or  accompanies  the  turning, 
is  not  represented.) 


240  THE    BEHAVIOR    OF    I.OWER    ORGANISMS. 

with  the  revolution  on  the  long  axis.  As  a  consequence,  the  anterior 
end  is  swung  about  in  a  wide  circle ;  the  organism  tries  successively 
many  widely  differing  directions  (Fig.  80).  From  each  of  these  direc- 
tions, as  we  have  seen,  a  sample  of  water  is  brought  to  the  sensitive 
anterior  end  or  mouth.  Thus  the  reaction  in  itself  consists  in  trying 
the  water  in  many  different  directions.  As  long  as  the  water  coming 
from  these  various  directions  evinces  the  qualities  which  caused  the 
reaction — the  greater  heat  or  cold  or  the  chemical — the  reaction,  with 
its  swinging  to  one  side,  continues.  When  a  direction  is  reached  from 
which  the  water  no  longer  shows  these  qualities,  there  is  no  further 
cause  for  reaction  ;  the  strong  swerving  toward  the  side  A' ceases,  and 
the  organism  swims  forward  in  the  direction  toward  which  it  is  now 
pointed.  It  has  thus  avoided  the  region  where  the  conditions  were 
such  as  to  produce  stimulation. 

While  the  account  just  given  shows  the  essential  features  of  the  reac- 
tion, the  actual  series  of  events  appears  in  many  cases  more  complicated, 
though  there  is  nothing  differing  in  principle  from  what  was  just  set 
forth.  The  apparently  greater  complication  arises  from  the  repetition 
of  that  feature  of  the  reaction  which  consists  in  swimming  backward, 
and  in  the  cessation  of  the  reaction  at  intervals,  with  an  attempt  to 
swim  forward.  After  the  organism  has  swung  the  anterior  end  to  one 
side,  if  it  still  receives  the  stimulus  it  may  begin  the  reaction  anew  ; 
that  is,  it  may  swim  backward  a  distance,  and  again  begin  turning 
toward  the  side  X.  This  may  be  repeated  several  times.  Each  time 
it  is  repeated  the  organism  swings  its  anterior  end  through  a  new  series 
of  positions,  thus  increasing  the  chances  of  finding  one  in  which  there 
is  no  farther  stimulation.  Again,  the  organism,  after  reacting  in  the 
way  described  in  the  last  paragraph,  may  begin  to  swim  forward,  only 
to  find  that  it  receives  the  stimulus  again  ;  it  then  repeats  the  whole 
reaction,  thus  supplying  itself  with  a  completely  new  set  of  directions 
and  of  samples  of  water  from  those  directions.  In  some  cases  the  reac- 
tion is  thus  repeated  many  times  before  any  direction  is  found  toward 
which  the  organism  can  swim  without  receiving  stimulation. 

This  is  the  method  of  behavior  which  the  present  author  has  been 
describing  in  detail  in  many  organisms  in  his  series  of  ten  Studies  on 
Reactions  to  Stimuli  in  Unicellular  Organisms,*  and  in  the  foregoing 
Contributions  to  the  Study  of  the  Behavior  of  the  Lower  Organisms. 
Not  until  recently,  it  must  be  confessed,  has  the  real  significance  of 
this  type  of  behavior  been  fully  perceived.  The  results  seemed  to  a 
large  degree  negative  ;  the  reaction  method  clearly  did  not  agree  with 
the  prevailing  tropism  theory,  nor  with  any  other  of  the  commonly 

♦Journ.  of  Physiol.,  1897,  vol.  21;  Amer.  Journ.  of  Physiol.,  vols.  2  to  8, 
1899  to  1902;  Amer.  Naturalist,  vol.  33,  1899;  Biol,  Bull.,  vol.  3,  190;. 


THE    METHOD   OF   TRIAL   AND    ERROR.  24I 

held  theories  as  to  the  reactions  of  lower  organisms.  Just  what  the 
organism  did  was,  indeed,  fairly  clear,  but  the  plan  of  it  all,  the  gen- 
eral relations  involved  in  all  the  details,  was  not  clear.  This  was 
partly  due,  perhaps,  to  overemphasis  of  certain  phases  of  the  reaction 
and  to  a  tendency  to  consider  other  features  unimportant.  The  beha- 
vior under  stimuli  is  a  unit ;  each  factor  must  be  considered  in  connec- 
tion with  all  the  others ;  then  the  general  method  running  through  it 
all  becomes  strikingly  evident. 

Let  us  now  return  to  the  organisms.  Sometimes  stimuli  are  received 
of  such  a  nature  that  their  distribution  is  not  affected  by  the  currents 
produced  by  the  cilia ;  in  other  words,  they  cannot  be  sampled  in  the 
currents  of  water  brought  to  the  anterior  end  or  mouth,  as  shown  in 
Figs.  79  and  80.  This  is  true,  for  example,  of  stimulation  by  light, 
and  of  stimulation  by  contact  with  solid  objects.  Under  such  stimula- 
tion the  behavior  is  nevertheless  still  by  the  method  of  trial  and  error. 
Let  us  consider  first  the  reaction  to  a  mechanical  stimulus. 

When  the  organism  comes  in  contact  with  a  mechanical  obstacle  the 
reaction  is  exactly  the  same  as  that  already  described.  It  swims  back- 
ward, swings  toward  the  side  X^  and  this,  with  the  revolution  on  the 
long  axis,  points  the  anterior  end  successively  in  many  different  direc- 
tions. The  organism  then  follows  one  of  these  directions.  If  this  leads 
against  the  obstacle,  the  reaction  is  repeated,  till  finally  a  direction  is 
found  in  which  the  obstacle  is  avoided. 

In  the  reaction  to  light,  as  it  occurs  in  Stentor  or  Euglena,  experi- 
ment shows  that  changes  in  the  intensity  of  illumination  at  the  sensi- 
tive anterior  end  are  the  agents  causing  reaction  (see  the  second  of  these 
contributions) .  The  reaction  produced  is  that  already  described  ;  by 
turning  toward  the  side  A^and  revolving  on  its  long  axis,  the  organism 
tries  many  directions. 

When  a  negative  organism,  such  as  Stentor,  comes  in  its  swimming 
to  an  area  that  is  more  brightly  illuminated,  or  when  a  positive  organ- 
ism, such  as  Euglena,  comes  to  an  area  that  is  less  brightly  illuminated, 
the  change  in  intensity  acts  as  a  stimulus.  The  organism  responds  in 
the  way  already  described  ;  it  backs  away,  then  tries  many  different 
directions  by  swinging  its  anterior  end  about  in  a  circle.  It  then 
starts  forward  in  one  of  these  directions.  If  this  does  not  lead  into  the 
area  causing  stimulation,  well  and  good  ;  if  it  does,  the  organism 
repeats  the  reaction,  trying  a  new  set  of  directions,  till  it  finds  one  that 
does  not  carry  it  to  the  area  causing  stimulation. 

When  light  coming  from  a  certain  direction  falls  upon  one  side  of  a 
swimming  infusorian,  the  spiral  path  followed,  of  course,  causes  the 
anterior  end  to  be  pointed  successively  in  different  directions.  As  a 
result,  the  illumination  of  the  anterior  end  is  repeatedly  changed,  since 


242  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

in  some  directions  it  is  pointed  more  nearly  toward  the  light,  in  others 
more  away  from  the  light,  so  as  to  be  partly  shaded  by  the  rest  of  the 
body.  These  changes  in  illumination  cause  the  reaction  ;  the  organism 
tries  pointing  in  various  directions.  When  it  comes  into  such  a  posi- 
tion that  the  anterior  end  is  no  longer  subjected  to  changes  in  intensity 
of  illumination,  it  continues  to  swim  forward  in  that  direction.  Such 
a  position  is  found  only  when  the  axis  of  the  spiral  path  is  in  the  direc- 
tion of  the  light  rays.  In  an  organism  which  reacts  when  the  intensity  of 
illumination  is  decreased,  such  a  position  is  stable  only  when  the  anterior 
end  is  directed  toward  the  source  of  light ;  in  an  organism  which  reacts 
when  the  intensity  of  illumination  is  increased,  only  when  the  anterior 
end  is  directed  away  from  the  source  of  light  (details  in  second  of  these 
contributions).  Thus  the  organism  tries  various  directions  till  one  is 
found  which  does  not  subject  it  to  changes  in  intensity  of  illumination 
at  the  anterior  end  ;  in  this  direction  it  swims  forward. 

The  reaction  which  produces  orientation  to  light  can  be  stated  more 
simply,  but  less  completely  and  accurately,  as  follows :  When  light 
coming  from  a  certain  direction  falls  upon  the  sensitive  anterior  end  of 
a  negative  organism,  such  as  Stentor,  this  causes  the  reaction  above 
described.  The  animal,  after  backing,  tries  a  new  set  of  directions, 
by  whirling  its  anterior  end  about  in  a  circle.  It  continues  or  repeats 
this  until  a  direction  is  found  in  which  the  light  no  longer  falls  on  the  sen- 
sitive anterior  end.  It  is  then  oriented  with  anterior  end  away  from  the 
source  of  light.  In  the  positive  organisms,  such  as  Euglena,  the  method 
of  reaction  is  the  same,  save  that  it  is  the  shading  of  the  anterior  end 
that  causes  the  reaction.  When  the  anterior  end  is  shaded  the  organ- 
ism reacts  in  the  usual  way.  It  tries  successively  many  different  direc- 
tions, by  whirling  its  anterior  end  about  in  a  wide  circle ;  when  the 
anterior  end  becomes  pointed  toward  the  source  of  light,  the  organism 
continues  forward  in  that  direction. 

In  those  infusoria  which  creep  along  the  bottom,  as  Stylonychia  or 
Oxytricha,  the  reaction  method  is  of  a  slightly  simpler  character, 
though  identical  in  principle.  These  animals  when  creeping  do  not 
rotate  on  the  long  axis.  When  stimulated  in  any  of  the  ways  described, 
they  dart  back,  then  turn  to  their  right.  They  thus  keep  in  contact 
with  the  bottom,  and  may  turn  through  any  number  of  degrees  up  to 
360  or  more  (Fig.  81).  The  reaction  places  them  thus  successively 
in  every  position  with  reference  to  the  source  of  stimulus  that  is  possi- 
ble so  long  as  they  remain  on  the  bottom,  and  in  each  position  the 
adoral  cilia  are  bringing  samples  of  water  to  the  anterior  end  and 
mouth,  as  in  Fig.  81.  When  a  position  is  reached  where  the  stimulus 
no  longer  acts,  the  reaction  ceases,  and  the  animal  moves  forward  in 
that  direction.  The  reaction  is  sometimes  repeated  several  times  before 
the  definitive  position  is  attained. 


THE    METHOD    OF   TRIAL   AND    ERROR. 


243 


In  no  other  group  of  organisms  does  the  method  of  trial  and  error 
so  completely  dominate  behavior,  perhaps,  as  in  the  infusoria.  In  this 
group  the  entire  organization  seems  based  on  this  method.  But  reac- 
tions on  this  plan  are  found  abundantly  elsewhere.  In  Amceba  the 
present  author  has  shown  that  many  of  the  reactions  are  of  this  charac- 
ter. (See  the  preceding  paper  on  the  movements  and  reactions  of 
Amoeba.)  When  stimulated  mechanically  or  by  a  chemical,  the 
Amoeba  does  not  move  directly  away  from  the  source  of  stimulus,  but 
merely  in  some  other  direction  than  that  toward  the  side  stimulated. 
If  this  leads  to  a  new  stimulus,  the  animal  tries  another  direction.  By 
continued  stimuli  Amoeba  may  be  driven  in  a  definite  direction.  The 
conditions  necessary  for  this  are  that  movement  in  any  other  direction 
shall  lead  to  stimulation. 

Reaction  on  the  plan  of  trial  and  error  is,  perhaps,  best  seen  in 
Amoeba  in  the  method  by  which 
a  specimen  suspended  in  the  water 
finds  and  attaches  itself  to  a  solid 
object.  The  suspended  Amoeba 
sends  out  pseudopodia  in  all  di- 
rections. If  the  tip  of  one  of  these 
pseudopodia  comes  in  contact  with 
a  solid  object  it  becomes  attached  ; 
the  protoplasm  begins  to  flow  in 
that  direction,  and  all  the  other 
pseudopodia  are  withdrawn.  The 
Amoeba  then  passes  to  the  solid 
and  creeps  over  its  surface.  Thus 
the  Amoeba  has  tried  sending  out  pseudopodia  in  all  directions ;  that 
which  has  been  successful  in  finding  a  solid  determines  the  direction  of 
movement. 

In  bacteria  the  reactions  to  light,  to  chemicals,  and  to  mechanical 
stimuli  are  essentially  like  those  of  the  infusoria.  The  details  as  to  the 
direction  of  turning,  etc.,  are  not  known,  owing  to  the  minuteness  of 
these  organisms.  But  the  essential  point  is  that  when  the  bacteria  are 
stimulated  effectively  they  change  the  direction  of  movement.  vSuch 
change  is  repeated  until  the  organisms  are  brought  into  a  position 
where  there  is  no  effective  stimulation.  The  behavior  is  clearly  that 
of  trial  and  error. 


Fig.  81.* 


*  Fig.  81.— Different  positions  occupied  in  the  usual  reaction  to  stimuli  in 
Oxytricha.  The  animal  swings  its  anterior  end  in  a  circle,  occupying  succes- 
sively positions  i,  2,  3,  4,  5,  6,  and  receiving  a  sample  of  water  from  each  direc- 
tion in  which  the  anterior  end  is  pointed.  When  the  stimulus  ceases  the  animal 
may  swim  forward  in  any  of  these  directions,  (The  backward  swimming  which 
precedes  or  accompanies  the  turning  toward  the  right  side  is  not  represented.) 


244  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

In  the  Metazoa  behavior  is  usually  not  that  of  trial  and  error  in 
so  elementary  a  form  as  is  found  in  the  organisms  thus  far  considered. 
The  higher  animals,  with  the  development  of  a  nervous  system  and 
other  bodily  differentiations,  have  usually  acquired  the  power  of  react- 
ing more  precisely  with  reference  to  the  localization  of  the  source  of 
stimulus.  They  more  often,  therefore,  turn  directly  toward  or  away 
from  the  source  of  stimulus,  a  preliminary  trial  of  different  directions 
being  unnecessary.  But  with  the  acquirement  of  many  reaction  possi- 
bilities, the  field  for  the  operation  of  the  method  of  trial  and  error  is 
greatly  broadened.  This  could  be  amply  illustrated  from  the  behavior 
of  certain  of  the  lower  Metazoa.  I  hope  to  develop  this  point  in  detail 
at  some  later  time.  Since  at  present  we  are  interested  chiefly  in  the 
lowest  organism,  I  shall  mention  here  only  a  few  cases  in  the  Metazoa. 

In  the  Rotifera  behavior  is,  under  many  conditions,  precisely  similar 
to  that  which  I  have  described  above  for  the  infusoria  (details  in  the 
third  of  these  contributions) ;  that  is,  the  behavior  is  an  example  of  the 
method  of  trial  and  error  in  a  very  pure  form. 

In  Hydra  we  find  the  method  of  trial  and  error  in  a  number  of 
features  of  the  behavior.  Since  a  general  paper  on  the  behavior  of 
Hydra  is  in  preparation,*  I  will  mention  only  one  or  two  points  that 
have  already  been  described.  If  we  observe  a  living,  unstimulated 
green  Hydra,  we  find  that  it  does  not  remain  at  rest.  If  the  Hydra  is 
extended  in  a  certain  direction,  after  one  or  two  minutes  it  contracts, 
bends  over  to  a  new  position,  then  extends  in  a  new  direction.  After 
about  two  minutes  it  contracts  again,  bends  into  a  still  different  posi- 
tion, and  again  extends.  This  process  is  repeated  at  fairly  regular 
intervals,  so  that  after  a  time  the  Hydra  has  tried  every  position  possi- 
ble in  its  present  place  of  attachment.  This  exploration  of  all  parts  of 
the  surrounding  region,  of  course,  aids  greatly  in  finding  food. 

Mast  (1903)  finds  that  when  Hydra  is  heated  from  one  side  it  does 
not  move  directly  away  from  the  source  of  heat,  but  merely  moves  in 
some  random  direction.  In  other  words,  the  animal  when  heated 
merely  tries  a  new  position. 

Moebius  (1873)  describes  the  reaction  of  a  large  mollusk  (Nassa)  to 
chemical  stimuli,  as  shown  when  a  piece  of  meat  is  thrown  into  the 
aquarium  containing  them.  They  do  not  orient  themselves  in  the  lines 
of  diffusion  and  travel  directly  toward  the  meat,  but  move  "  now  to  the 
right,  now  to  the  left,  like  a  blind  man  who  guides  himself  forward  by 
trial  with  his  stick.  In  this  way  they  discover  whether  they  are  com- 
ing nearer  or  going  farther  away  from  the  point  from  which  the  attrac- 
tive stimulus  arises"  (/.  c,  p.  9,  translation).  The  reaction  is  thus  a 
clear  case  of  the  method  of  trial  and  error.     Experiments  on  the  leech, 

*  By  Mr.  George  Wagner. 


THE    METHOD    OF   TRIAL   AND    ERROR.  245 

by  Miss  Frances  Dunbar,  which  I  hope  may  soon  be  published,  show 
that  that  animal  finds  its  food  in  a  similar  manner.  All  searching  is, 
of  course,  behavior  on  the  plan  of  trial  and  error,  and  many  organisms 
are  known  to  search  for  food. 

The  righting  reactions  of  organisms  are  among  the  most  striking 
examples  of  trial  and  error  in  behavior.  In  the  starfish,  for  example, 
when  the  animal  is  laid  on  its  back  "  the  tube  feet  of  all  the  arms  are 
stretched  out  and  are  moved  hither  and  thither,  as  if  ieeling  for  some- 
thing, and  soon  the  tips  of  one  or  more  arms  turn  over  and  touch  the 
underlying  surface  with  their  ventral  side  "  (Loeb,  1900,  p.  62).  As 
soon  as  these  one  or  two  arms  have  been  successful,  the  others  cease 
their  eflforts ;  the  attached  arms  then  turn  the  body  over.  If  all  the 
arms  attempted  to  turn  the  animal  at  the  same  time,  in  other  words,  if 
there  were  no  way  of  recognizing  "  success  "  in  the  trial,  the  animal 
could  not  right  itself. 

The  righting  reaction  of  the  starfish  shows  much  resemblance  to  the 
method,  described  above,  by  which  a  suspended  Amoeba  passes  to  a 
solid.  It  is  probable  that  a  Difflugia,  turned  with  the  opening  of  the 
shell  upward,  would  show  a  righting  reaction  essentially  similar  to 
that  of  the  starfish. 

The  righting  reaction  of  the  flatworm  Planaria,  as  described  by  Pearl 
(1903),  is  not  so  evidently  brought  about  through  the  method  of  trial 
and  error.  Yet  there  are  certain  facts  that  indicate  that  this  method  is 
really  essentially  present  here.  Thus,  Pearl  shows  that  when  the  flat- 
worm  is  prevented  from  righting  itself  in  the  usual  way,  its  rights  itself 
in  another  manner.  Probably  various  reactions  are  tried  ;  if  the  first 
does  not  succeed  another  may. 

This  peculiar  form  of  the  method  of  trial  and  error,  in  which  several 
different  reactions  are  tried  even  under  but  a  single  stimulus,  is  brought 
out  by  Mast  (1903)  in  the  behavior  of  Planaria  under  other  conditions. 
If  the  water  containing  the  flatworms  is  heated,  the  animals  give,  as  the 
temperature  rises,  practically  all  the  reactions  that  they  ever  give  under 
any  conditions. 

We  have  thus,  as  the  temperature  rises  and  the  stimulation  increases,  the  fol- 
lowing reactions  given  consecutively:  positive,  negative,  crawling,  righting, 
and  final  (all  the  reactions  described  by  Pearl,  with  the  exception  of  the  food 
reactions,  and  the  final  reaction  in  addition).     (Mast,  1903,  p.  185.) 

We  shall  have  occasion  to  inquire  as  to  the  significance  of  this 
responding  to  the  same  stimulus  by  many  different  reactions  when  we 
take  up,  in  another  connection,  certain  similar  phenomena  in  Stentor. 

In  the  higher  vertebrates,  as  we  have  mentioned  at  the  beginning, 
the  method  of  trial  and  error  plays  a  very  large  part.  It  is  here  espe- 
cially that  it  has  been  recognized  as  a  definite  type  of  behavior  in  the 


246  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

work  of  Lloyd  Morgan,  Thorndike,  and  others.    With  the  details  of  its 
manifestations  in  higher  animals  we  need  not  concern  ourselves  here. 

Let  us  now  return  to  the  method  of  trial  and  error  in  the  infusoria. 
Here  it  is  most  strongly  marked,  and  certain  general  problems  which 
arise  from  it  are  sharply  defined.  It  is  possible  to  formulate  the  reac- 
tion method  of  the  infusoria  as  follows :  When  effectively  stimulated 
by  agents  of  almost  any  sort  the  organism  moves  backward,  and  turns 
toward  a  structurally  defined  side  X^  while  at  the  same  time  it  may 
continue  to  revolve  on  its  long  axis.  As  thus  stated,  the  reaction 
method  seems  exceedingly  simple  and  stereotyped,  and  as  such  I  pre- 
sented the  behavior  of  these  organisms  in  a  former  general  paper.*  If 
we  limit  ourselves  to  a  consideration  of  the  reaction  itself,  this  seems 
inevitable,  although  certain  additional  reactions  have  been  described 
since  that  paper  was  written.  But  when  we  study  the  relation  of  this 
reaction  method  to  the  environmental  conditions,  the  results  are  most 
remarkable,  and  a  totally  new  set  of  problems  appears.  Whether  the 
behavior  is  to  be  called  simple  and  stereotyped,  or  complicated  and 
flexible,  is  not  so  easy  to  decide.  The  relations  of  the  reaction  of  the 
environmental  conditions  are,  perhaps,  the  really  essential  point  in 
animal  behavior.  What  are  the  relations  which  we  find  in  the  organ- 
isms reacting  in  the  way  set  forth  above } 

In  general  terms  we  find  that  through  this  reaction  by  trial  and  error 
the  organisms  are  kept  in  conditions  favorable  to  their  existence,  and 
prevented  from  entering  unfavorable  regions.  Through  it  they  keep 
out  of  hot  and  cold  regions  and  collect  in  regions  of  moderate  temper- 
ature. Through  it  they  tend  to  keep  out  of  strong  or  injurious  chemi- 
cals and  out  of  regions  where  the  osmotic  pressure  is  much  above  or 
below  that  to  which  they  are  accustomed.  Through  it  they  gather  in 
regions  containing  small  amounts  of  certain  chemicals,  not  leaving 
them  for  regions  where  there  is  either  more  or  less  of  these  chemicals. 
When  oxygen  is  needed  they  collect  through  this  reaction  in  regions 
containing  oxygen ;  when  the  oxygen  pressure  is  high,  they  do  not 
react  with  reference  to  oxygen,  or  through  this  reaction  they  avoid 
regions  containing  much  oxygen.  Through  this  reaction  organisms 
which  contain  chlorophyll,  and  therefore  need  light,  gather  in  lighted 
regions  or  move  toward  the  source  of  light  ;  through  the  same  reaction 
the  same  organisms  avoid  very  powerful  light.f     In  all  these  cases. 


*  Psychology  of  a  Protozoan,  Amer.  Journ.  Psychol.,  vol.  10,  1899.  pp.  503-515. 

t  For  details,  see  the  author's  Studies,  already  referred  to,  and  the  preceding 
contributions.  In  papers  by  Engelmann  (1882,  a)  and  Rothert  (1901)  the  reac- 
tion method  involved  is  also  described  for  certain  organisms,  though  these 
writers,  like  the  present  author  in  his  earlier  papers,  did  not  bring  out  the  rela- 
tions to  a  general  method  of  trial  and  error.  Engelmann,  however,  character- 
ized the  reaction  of  Euglena  to  light  directly  as  a  "  Probiren" — a  "  trial." 


THE    METHOD    OF   TRIAL   AND    ERROR.  247 

when  there  is  error  the  organism  goes  back  and  tries  a  new  direction, 
or  a  whole  series  of  new  directions. 

But  what  constitutes  "error"  ?  This  is  a  fundamental  question  for  this 
method  of  behavior.  Why  does  the  organism  react  to  some  things  by 
turning  away  and  trying  new  directions,  to  others  not?  Why  do  they 
react  thus  on  coming  to  certain  chemicals,  and  on  leaving  others.? 
Why  do  they  react  thus  on  coming  to  a  strong  chemical,  and  also  on 
leaving  a  weak  solution  of  the  same  chemical?  Why  does  the  same 
organism  react  thus  to  strong  light,  and  also  to  darkness?  To  heat 
and  also  to  cold?  What  decides  whether  a  certain  condition  is  '*  er- 
ror '*  or  not?  A  list  of  all  the  different  agents  that  must  be  considered 
"  error"  from  the  standpoint  of  this  reaction  method  reveals,  so  far  as 
chemical  or  physical  classification  is  concerned,  a  most  heterogeneous 
and  even  contradictory  collection.  What  is  the  common  factor  which 
makes  them  all  error? 

Examination  shows  that  error  from  the  standpoint  of  this  behavior 
is  as  a  rule  error  also  from  the  standpoint  of  the  general  interests  of 
the  organism,  considering  as  the  interests  of  the  organism  the  perform- 
ance of  its  normal  functions,  the  preservation  of  its  existence,  and  the 
production  of  posterity.  In  general  the  organism  reacts  as  error  to 
those  things  which  are  injurious  to  it,  while  in  those  conditions  which 
are  beneficial  it  continues  its  normal  activities.  There  are  some  excep- 
tions to  this,  but  in  a  general  view  it  is  clearly  evident.  There  is  no 
common  thread  running  through  all  the  different  agents  which  consti- 
tute '*  error"  in  the  reactions,  save  this  one,  that  they  are  error  from 
the  standpoint  of  the  general  interests  of  the  organism. 

How  can  we  account  for  the  fact  that  these  lowest  organisms  react 
to  all  sorts  of  things  that  are  injurious  to  them  by  a  reaction  which 
tends  to  remove  them  from  the  action  of  the  agent, — by  a  negative  reac- 
tion? The  first  response  to  this  question  must  be  another  question. 
How  can  we  account  for  the  fact  that  in  man  we  have  the  same  condi- 
tion of  affairs?  How  does  it  happen  that  we  respond  by  drawing  back 
both  from  flame  and  from  ice,  though  these  act  physically  in  opposite 
ways?  Why  do  we  seek  light,  but  avoid  a  blinding  glare?  Why  do 
we  receive  without  opposition  certain  chemical  stimuli  (odors  and 
tastes)  and  avoid  others?  The  facts  are  quite  parallel  in  man  and  in 
the  lowest  organisms  in  these  respects.  In  man  certain  stimuli  cause 
reactions  which  tend  to  remove  the  organism  from  the  source  of  the 
stimulus  (negative  reactions),  while  others  have  the  opposite  effect; 
this  is  true  also  of  Euglena  and  Paramecium.  In  both  cases  the  stimuli 
which  produce  the  negative  reaction  form  a  heterogeneous  collection 
from  the  chemical  or  physical  standpoint.  In  both  cases  the  stimuli 
producing  the  negative  reaction  are  in  general  injurious  to  the  organism. 
The  problem  is  one  for  the  highest  and  for  the  lowest  organisms. 


248  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

In  ourselves  the  stimuli  which  induce  the  negative  reaction  bring 
about  the  subjective  state  known  as  pain  (in  varying  degrees,  from  dis- 
comfort or  dislike  to  anguish),  and  popularly  we  consider  that  the  draw- 
ing back  is  due  to  the  pain.  Is  there  ground  for  this  view?  Or  is  the 
reaction  entirely  accounted  for  by  the  chemical  and  physical  processes 
involved?  When  the  burnt  child  draws  its  hand  back  from  the  flame, 
does  the  state  of  consciousness  called  pain  have  anything  to  do  with 
the  reaction  ? 

Without  attempting  to  answer  this  question,  we  wish  to  point  out 
the  bearing  of  possible  answers  on  our  problem  in  the  lower  organisms. 
If  we  hold  that  in  man  we  cannot  account  for  the  reaction  without  tak- 
ing into  consideration  the  pain,  then  we  must  hold  to  the  same  view 
for  the  lower  organisms.  If  we  maintain  that  in  man  we  cannot 
account  for  the  selection  of  such  a  heterogeneous  group  of  conditions  for 
the  negative  response — conditions  seeming  to  have  nothing  in  common 
save  that  they  cause  pain — without  taking  into  consideration  the  pain, 
then  we  are  forced  to  the  same  conclusion  in  the  unicellullar  organisms, 
for  here  we  have  a  precisely  parallel  series  of  phenomena.  Anyone, 
then,  who  holds  that  pain  is  a  necessary  link  in  the  chain  of  events  in 
man  must  consider  that  we  are  undertaking  a  hopeless  task  in  trying  to 
account  for  the  reactions  of  the  lower  organisms  purely  from  the  chem- 
ical and  physical  conditions.  And  the  converse  is  also  true.  Anyone 
who  holds  that  we  can  account  fully  for  the  reactions  of  Euglena  or 
Paramecium,  purely  from  the  physico-chemical  conditions,  without 
taking  into  account  any  states  of  consciousness,  must  logically  hold  that 
we  can  do  the  same  in  man.  The  method  of  trial  and  error  implies 
some  way  of  distinguishing  error  ;  the  problem  is  :  How  is  this  done? 
The  problem  is  one,  so  far  as  objective  evidence  goes,  throughout  the 
animal  series. 

We  can,  of  course,  know  nothing  of  pain  in  any  organism  except 
the  self,  and  we  can,  in  a  purely  formal  way  at  least,  solve  our  problem 
equally  well  (or  equally  ill)  without  taking  pain  directly  into  consider- 
ation. Even  in  man  we  must  hold  that  pain  is  preceded  or  accom- 
panied in  every  case  by  a  certain  physiological  condition.  And  if  there 
is  something  common  to  all  states  of  pain,  it  would  appear  that  there 
must  be  something  common  to  all  the  physiological  states  accompany- 
ing or  preceding  pain.  We  thus  get  a  common  basis  for  all  the  nega- 
tive reactions ;  if  they  are  preceded  or  accompanied  by  a  common 
physiological  state,  this  state  will  serve  formally  as  an  explanation  for 
the  common  reaction,  fully  as  well  as  would  a  common  state  of  con- 
sciousness. The  facts  could  be  formulated  as  follows  :  In  any  animal, 
from  the  lowest  up  to  man,  a  certain  heterogeneous  set  of  agents,  which 
are  in  general  injurious,  produce  a  certain  physiological  state,  common 


THE    \CETHOD    OF    TRIAL    AND    ERROR.  249 

to  all ;  as  a  consequence  or  concomitant  of  this  physiological  state  a 
negative  reaction  follows.  In  man  this  physiological  state  is  accom- 
panied by  pain.  The  common  physiological  state  might  then  properly 
receive  a  name  which  brings  out  its  relation  to  the  state  accompanied 
in  man  by  pain ;  for  example,  J.  Mark  Baldwin's  *'  organic  analogue 
of  pain.'' 

We  have  left  under  this  formulation  the  fundamental  question  as  to 
how  a  set  of  agencies  that  are  quite  heterogeneous  from  a  chemical  or 
physical  standpoint  can  produce  a  common  physiological  state.  This 
question  is,  of  course,  of  precisely  the  same  order  of  difficulty  as  that 
which  asks  how  the  same  heterogeneous  set  of  agents  can  produce  a 
common  state  of  consciousness,  namely,  pain.  We  therefore  lose  noth- 
ing, so  far  as  this  problem  is  concerned,  by  substituting  '•'•  a  common 
physiological  state"  for  "pain"  in  dealing  with  the  subject.  But  to 
attempt  to  deal  with  the  problem  of  negative  reactions  in  the  lower 
organisms  without  recognizing  that  they  are  conditioned  in  the  same 
way  as  the  negative  reactions  of  man — without  admitting  the  existence 
of  some  physiological  state  analogous  to  that  which  is  accompanied  by 
pain  in  man,  is,  I  believe,  to  close  one's  eyes  to  patent  realities. 

We  have  seen  above  that  the  method  of  trial  and  error  involves  some 
way  of  distinguishing  error.  But  do  not  some  of  the  facts  indicate 
that  it  involves,  at  least  sometimes,  also  some  way  of  distinguishing  the 
opposite  of  error  ;  that  is,  what  we  may  call  success.^  For  most  of  the 
reactions  of  the  infusoria  this  seems  not  necessary,  for  what  the  organ- 
ism does  when  successful  is  merely  to  continue  the  condition  in  which 
it  finds  itself  at  the  time.  There  is  then  no  objective  evidence  that  a 
stimulus  is  acting  at  this  time.  In  these  organisms  it  seems  to  be  chiefly 
the  injurious  or  negative  stimuli  that  induce  a  motor  reaction.  But 
consider  the  floating  Amceba,  which  sends  forth  pseudopodia  in  all 
directions.  Finally  one  of  these  pseudopodia  comes  in  contact  with 
a  solid,  and  to  this  stimulus  the  Amceba  reacts  positively.  Now  all 
the  other  pseudopodia,  though  the  external  conditions  directly  affecting 
them  remain  the  same,  become  retracted,  and  the  whole  Amceba  moves 
toward  the  pseudopodium  in  contact.  This  withdrawal  of  the  other 
pseudopodia  requires  for  its  explanation  a  change  in  physiological  state 
which  can  be  due  only  to  the  success  of  the  pseudopodium  that  has 
come  in  contact  with  a  solid.  There  is  certainly  no  basis  here  for  con- 
sidering the  reaction  as  due  to  an  "  organic  analogue  of  pain"  ;  possi- 
bly a  case  could  be  made  out,  on  the  other  hand,  for  a  physiological 
state  corresponding  to  that  which  conditions  pleasure  in  ourselves. 
Possibly  similar  considerations  hold  for  the  positive  reactions  of  other 
organisms — infusoria,  etc. — to  solids. 

There  appears  to  be  a  similar  state  of  affairs  in  the  righting  reaction. 


250  THE    BEHAVIOR   OP   LOWER    ORGANISMS. 

When  the  starfish  is  placed  on  its  back,  the  physiological  state  existing 
induces  all  the  arms  to  initiate  feeling  movements ;  the  animal  tries  to 
reach  a  solid  with  its  tube  feet.  As  soon  as  one  or  two  arms  have  suc- 
ceeded, this  success  is  recognized  by  the  cessation  of  effort  on  the  part 
of  the  other  arms.  Their  physiological  state  has  changed  to  one  cor- 
responding to  success. 

We  may  sum  up  our  discussion  on  these  points  as  follows :  The 
method  of  trial  and  error  involves  some  way  of  distinguishing  error, 
and  also,  in  some  cases  at  least,  some  method  of  distinguishing  success. 
The  problem  as  to  how  this  is  done  is  the  same  for  man  and  for  the 
infusorian.  We  are  compelled  to  postulate  throughout  the  series  cer- 
tain physiological  states  to  account  for  the  negative  reactions  under 
error,  and  the  positive  reactions  under  success.  In  man  these  physio- 
logical states  are  those  conditioning  pain  and  pleasure. 

The  *'  method  of  trial  and  error,"  as  this  phrase  is  used  in  the 
present  paper,  is  evidently  the  same  as  reaction  by  "  selection  of  over- 
produced movements,"  which  plays  so  large  a  part  in  the  theories  of 
Spencer  and  Bain  and  especially  in  the  recent  discussions  of  behavior 
by  J.  Mark  Baldwin.  To  this  aspect  of  the  matter  the  present  writer 
will  return  in  the  future. 

This  method  of  trial  and  error,  which  forms  the  most  essential  feature 
of  the  behavior  of  these  lower  organisms,  is  in  complete  contrast  with 
the  tropism  schema,  which  has  long  been  supposed  to  express  the 
essential  characteristics  of  their  behavior.  The  tropism  was  conceived 
as  a  fixed  way  of  acting,  forced  upon  the  organism  by  the  direct  action 
of  external  agents  upon  its  motor  organs.  Each  class  of  external  agents 
had  its  corresponding  tropism  ;  under  its  action  the  organism  performed 
certain  forced  movements,  usually  resulting  in  its  taking  up  a  rigid 
position  with  reference  to  the  direction  from  which  the  stimulus  came. 
Whether  it  then  moved  toward  or  away  from  the  source  of  stimulus 
was  determined  by  accidental  conditions,  and  played  no  essential  part 
in  the  reaction.  There  was  no  trial  of  the  conditions  ;  no  indication 
of  anything  like  what  we  call  choice  in  the  higher  organisms ;  the 
behavior  was  stereotyped.  Doubtless  such  methods  of  reaction  do 
exist.  In  the  reactions  of  infusoria  to  the  electric  current  (an  agent 
with  which  they  never  come  into  relation  in  nature),  there  are  cer- 
tain features  which  fit  the  tropism  schema,  and  in  the  instincts — the 
''  Triebe" — of  animals  there  are  features  of  this  stereotyped  character. 
The  behavior  of  animals  is  woven  of  elements  of  the  most  diverse  kind. 
But  certainly  in  the  lower  organisms  which  we  have  taken  chiefly  into 
consideration  the  behavior  is  not  typically  of  the  stereotyped  character 
expressed  in  the  tropism  schema.  The  method  of  trial  and  error  is 
flexible ;  indeed,  plasticity  is  its  essential  characteristic.     Working  in 


THE    METHOD    OF   TRIAL   AND    ERROR.  25 1 

the  lowest  organisms  with  very  simple  factors,  it  is  nevertheless  capable 
of  development ;  it  leads  upward.  The  tropism  leads  nowhere  ;  it  is 
a  fixed,  final  thing,  like  a  crystal.  The  method  of  trial  and  error  on 
the  other  hand  has  been  called  the  ''method  of  intelligence"  (Lloyd 
Morgan,  1900,  p.  139)  ;  it  involves  in  almost  every  movement  an 
activity  such  as  we  call  choice  in  higher  organisms.  With  the  acquire- 
ment of  2i  finer  perception  of  differences  the  organism  acting  on  the 
method  of  trial  and  error  rises  at'once  to  a  higher  grade  in  behavior. 
Combining  this  with  the  development  of  sense  organs  and  the  diflferen- 
tiation  of  motor  apparatus,  the  path  of  advancement  is  wide  open 
before  it. 

The  most  important  step  in  advance  is  that  shown  when  the  results 
of  one  reaction  by  trial  and  error  become  the  basis  for  a  succeeding 
reaction.  The  method  of  reacting  which  leads  to  success  is  determined 
by  trial ;  after  it  is  once  or  several  times  thus  determined,  the  trials  are 
omitted,  and  the  organism  at  once  performs  the  successful  action. 
This  is  intelligence^  according  to  Lloyd  Morgan  (1900,  p.  138),  and 
it  is  as  leading  to  this  result  that  the  method  of  trial  and  error  can  be 
characterized  also  as  the  method  of  intelligence.  In  intelligent  action, 
while  the  organism  must  react  the  first  time  by  the  method  of  trial  and 
error,  it  need  not  begin  all  over  again  each  time  the  same  circumstances 
are  presented.  Do  we  find  any  indication  of  such  action  among  uni- 
cellular organisms? 

In  Stentor  we  find  action  of  this  character  to  a  certain  extent.  It 
does  not  continue  reacting  strongly  to  a  stimulus  that  is  not  injurious, 
but  after  a  time,  when  such  a  stimulus  is  repeated,  it  ceases  to  react, 
or  reacts  in  some  less  pronounced  way  than  at  first.  To  an  injurious 
stimulus,  on  the  other  hand,  it  does  continue  to  react,  but  not  through- 
out in  the  same  manner.  When  such  a  stimulus  is  repeated,  Stentor 
tries  various  different  ways  of  reacting  to  it.  If  the  result  of  reacting 
by  bending  to  one  side  is  not  success,  it  tries  reversing  the  ciliary  cur- 
rent, then  contracting  into  its  tube,  then  leaving  its  tube,  etc.  (details 
in  Jennings,  1902,  a).  This  is  clearly  the  method  of  trial  and  error 
passing  into  the  method  of  intelligence,  but  the  intelligence  lasts  for 
only  very  short  periods.  To  really  modify  the  life  of  the  organism  in 
any  permanent  way,  as  happens  in  higher  animals,  the  method  of 
reacting  discovered  to  be  successful  by  the  method  of  trial  and  error 
should  persist  for  a  long  time.  Apparently  this  is  not  the  case  for 
unicellular  organisms,  but  further  work  is  needed  on  this  point. 

An  application  of  the  method  of  trial  and  error  similar  to  that  of 
Stentor  is  found  under  certain  circumstances  in  the  flatworm.  Pearl 
(1903)  found  that  after  the  animal  had  reacted  to  a  repeated  mechanical 
stimulus  for  a  long  time  by  turning  away  from  it,  it  suddenly  reversed 


252  THE    BEHAVIOR    OF   LOWER    ORGANISMS. 

the  reaction,  and  turned  far  toward  the  side  on  which  the  stimulus  was 
acting.  Mast  (1903)  showed,  as  we  have  seen,  that  when  the  flatworm 
is  heated  it  tries  successively  almost  every  form  of  reaction  which  it 
has  at  command.  Such  results  have  a  most  important  bearing  on  the 
problem  of  the  relation  of  the  reaction  method  to  the  stimulus.  Neither 
direct  action  of  the  stimulus  on  the  motor  organs  as  separate  entities, 
nor  a  typical  fixed  interconnection  of  sense  organs  and  motor  organs 
can  explain  such  results.  As  a  result  of  continued  strong  stimulation 
the  organism  passes  from  one  physiological  state  to  another,  and  each 
physiological  state  has  its  concomitant  method  of  reaction. 

The  present  paper  may  be  considered  as  the  summing  up  of  the 
general  results  of  several  years'  work  by  the  author  on  the  behavior  of 
the  lowest  organisms.  This  work  has  shown  that  in  these  creatures 
the  behavior  is  not  as  a  rule  on  the  tropism  plan — a  set,  forced  method 
of  reacting  to  each  particular  agent — but  takes  place  in  a  much  more 
flexible,  less  directly  machine-like  way,  by  the  method  of  trial  and 
error.  This  method  involves  many  of  the  fundamental  qualities  which 
we  find  in  the  behavior  of  higher  animals,  yet  with  the  simplest  possi- 
ble basis  in  ways  of  action  ;  a  great  portion  of  the  behavior  consisting 
often  of  but  one  or  two  definite  movements,  movements  that  are  stereo- 
typed when  considered  by  themselves,  but  not  stereotyped  in  their 
relation  to  the  environment.  This  method  leads  upward,  offering  at 
every  point  opportunity  for  development,  and  showing  even  in  the 
unicellular  organisms  what  must  be  considered  the  beginnings  of  intel- 
ligence* and  of  many  other  qualities  found  in  higher  animals.  Tropic 
action  doubtless  occurs,  but  the  main  basis  of  behavior  is  in  these 
organisms  the  method  of  trial  and  error. 

♦Throughout  this  paper  a  number  of  terms  are  used  whose  significance  as 
they  are  commonly  employed  is  determined  by  our  subjective  experience.  But 
all  these  terms  (save  those  directly  characterized  as  "  subjective  states,"  or 
"states  of  consciousness")  will  be  found  susceptible  also  of  definition  from  cer- 
tain objective  manifestations,  and  it  is  in  this  objective  sense  that  they  are  used 
in  the  present  paper.  Thus  *'  perception  "  of  a  stimulus  means  merely  that  the 
organism  reacts  to  it  in  some  way ;  "  discrimination  "  of  two  stimuli  means  that 
the  organism  reacts  differently  to  them  ;  "  intelligence  "  is  defined  by  the  objective 
manifestations  mentioned  in  the  text,  etc.  These  terms  are  employed  because  it 
would  involve  endless  circumlocution  to  avoid  them;  they  are  the  vocabulary 
that  has  been  developed  for  describing  the  behavior  of  men,  and  if  we  reject  them, 
it  is  almost  impossible  to  describe  behavior  intelligibly.  When  their  objective 
significance  is  kept  in  mind  there  is  no  theoretical  objection  to  them,  and  they 
have  the  advantage  that  they  bring  out  the  identity  of  the  objective  factors  in  the 
behavior  of  animals  with  the  objective  factors  in  the  behavior  of  man. 


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1894.  Beobachtungen  Uber  den  Lichtsinn  augenloser  Muscheln.  Biol.  Cen- 
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OSTWALD,  WiLHELM. 

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1903.  Zur  Theorie  der  Richtungsbewegungen  schwimmender  niederer  Organ- 

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1890.  Etudes  sur  les  Rhizopodes  d'eau  douce.     M6m.  de  la  Soc.  de  Physique 

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1888.     UeberperiodischeAusbreitung  von  Fliissigkeitsoberflachen  und  dadurch 

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256  THE   BEHAVIOR   OF   LOWER    ORGANISMS. 

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1891.  Die  physiologische  Bedeutung  des  Zellkernes.    Arch.  f.  d.  ges.  Physiol., 

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1895.     Allgemeine  Physiologie.     Ein  Grundriss  der  Lehre  vom  Leben.     584 

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1900.  On  the  eye-spot  and  flagellum  of  Englena  viridis.    Journ.  Lin.  Soc. 

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1902.  Zur  Kenntnis  der  Galvanotaxis.     Zeitschr.  f.  allg.  Physiol.,  Bd.  2,  pp. 

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Wallich,  G.  C. 

1863  a.  Further  observations  on  an  undescribed  indigenous  Amoeba,  with 
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1863  c.  Further  observations  on  the  distinctive  characters,  habits,  and  repro- 
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Yerkes,  R.  M. 

1900.  Reactions  of  Entomostraca  to  stimulation  by  light.  II.  Reactions  of 
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